Lab notebook: the great hammerhead (Sphyrna mokarran)

Lab 1

Specific objectives:

  • Document the external anatomy of the specimen
  • Identify the specimen using taxonomic features

The great hammerhead (Sphyrna mokarran) is from the family Sphyrnidae of the “ground sharks” or Carcharhiniformes [1] (Fig. 1).

Figure 1 External morphology of the great hammerhead shark, (Sphyrna mokarran)

The sheer size of S. mokarran hints at its predatory nature. Its serrated, pointed teeth are excellent for tearing apart flesh from prey like fish and rays, or perhaps crushing shells of crustaceans too [2], [3]. The ampullae of Lorenzini, located on the underside of its snout, are electroreceptors in the form of a network of mucus-filled pores helping in prey detection [4]. Its head’s unique “hammer” shape is called a cephalofoil, a unique evolution to enhance the shark’s vision. The position of the eyes on the ends of the cephalofoil allow the shark to always see above and below itself [5]. The cephalofoil also increases surface area for distribution of the ampullae of Lorenzini, thereby allowing the shark to locate prey more effectively [6]. The cephalofoil acts as a lifting surface, similar to the hydrofoil of a boat, and assists with sharp turns to attack prey [3], [7]. The two nares under the snout act as nostrils where water can pass through, allowing the shark to “smell” and assist with prey detection. The shape of the head means the nares are located further apart which may enhance olfaction.

The two dorsal, pelvic, and anal fins act as vertical stabilisers (in males, the pelvic fin is modified into a reproductive organ known as a clasper). The two pectoral fins help to steer while swimming and, like a plane, provide lift in the water. The caudal fin provides thrust, and the caudal fin of S. mokarran has a smaller lower lobe than the upper lobe, indicating that it may spend much time swimming close to the seabed and that speed is not as essential for this species. S. mokarran likely has carangiform or thunniform propulsion because of the large, muscular tail.

The colouration of S. mokarran is known as countershading, whereby the top surface is darker than the lighter underside. This means that the shark is camouflaged from prey above it (looking down to the deep, dark ocean) and from prey below it (looking up at the light, sunlight, surface waters). This will help the shark ambush its prey effectively and, for younger/smaller individuals, avoid detection from carnivores looking for a hammerhead-shaped snack. Its skin is comprised of dermal denticles: rough, teeth-like scales that would help reduce swimming-induced drag and protect them from predators and parasites. The lateral line extends the length of the shark sides and helps orient the shark to movement and sound. As a sensory organ, it works in conjunction with the ampullae of Lorenzini to assist in prey detection.

Lab 2

Specific objective:

  • Describe the functions of its organs as it relates to the ecology/biology of the specimen

Sharks lack an operculum and instead have gill slits that act as openings to the gills [8], allowing seawater to flow over them and oxygen to be extracted for respiration. From viewing photographs of S. mokarran, it does not appear to have a spiracle, like other sharks do (except requiem sharks). The spiracle is a small hole behind the eye that opens to the buccal cavity, assisting sharks to take in water over their gills whilst stationary, suitable for sharks that spend much time on the seafloor [9]. The lack of a spiracle coincides with the pelagic nature of S. mokarran and infers that they must be ram ventilators who must continuously swim forward to encourage water flow over the gill filaments through the mouth or gill slits [9].

Elasmobranchs are unique in that the morphological structure of their jaw means that it is suspended by a musculoskeletal sling [10]. S. mokarran are even more unique in that their head is dorsoventrally compressed and laterally expanded to form the cephalofoil. Because the evolution of the cephalofoil is such a drastic, morphological difference among Carcharhiniforms, trade-offs have been made to the pharyngeal apparatus (as well as other systems that occupy the head) [11]. Additionally, the teeth are triangular and serrated (Fig. 2).

One observation [7] of S. mokarran predation on a stingray saw the shark use its cephalofoil to pin the ray to the seafloor on two occasions, each time taking a bite from the wings of the ray, rendering it incapacitated. The hammerhead was then able to consume the immobile ray easily.

Figure 2 Teeth in dried jaws of great hammerhead shark, Sphyrna mokarran. Doug Perrine. (2013). received from https://www.alamy.com/stock-photo-teeth-in-dried-jaws-of-great-hammerhead-shark-sphyrna-mokarran-on-130546748.html on 29 September 2021.

There is limited research on S. mokarran digestion specifically, so it is helpful to infer similar characteristics from other species with a similar diet. The digestive tract begins at the mouth, where a strong jaw and sharp, replaceable teeth can rip flesh or crush prey into swallowable sizes. This is where the first type of digestion takes place – mechanical.

Food travels through the oesophagus from the mouth, where striated muscles and secreted mucous assist food into the stomach [12]. The stomach of most sharks is J-shaped [13], although there are some exceptions. The bonnethead shark (Sphyrna tiburo) exhibits a straight (I-shaped) stomach [14]. Because S. tiburo is from the same genus as S. mokarran, it may seem wise to assume that S. mokarran has an I-shaped stomach too, but S. tiburo is omnivorous and digests seagrass, whereas S. mokarran is strictly carnivorous. Like other vertebrates, the cells on the stomach walls of an elasmobranch secrete mucous to protect it from the acidic gastric juices that biochemically digest food stored in the stomach [12]. Some sharks are known to undergo gastric evacuation, whereby undigestible contents of the stomach are regurgitated out of the mouth [11], [12], although it is unknown is S. mokarran can do this. Furthermore, some elasmobranch species can regulate gastric acid secretion, likely in times of fasting due to low prey availability [15].

Nutrients are transported to the intestine from the stomach, which is relatively shorter than most vertebrate intestines. Leigh et al. (2017) recommend separating elasmobranch intestines into three sections: proximal, spiral, and distal. The proximal region gives way to the spiral region or spiral valve. The anatomy of the spiral valve varies among species but can have between 2–50 turns and is thought to increase surface area for absorption of nutrients and/or slow the rate at which food travels through the intestine, therefore, increasing time available for digestion [14], [16]. Furthermore, the spiral valve ensures that oversized items (e.g., bones) cannot pass through their lower intestine and allows them to be sufficiently broken down first or regurgitated.

After the spiral valve is the distal intestine, characterised by thicker and more muscular walls to accommodate the accumulation of faeces [12]. As pressure increases on the rectal walls, nerve impulses are sent to the brain for muscles to relax, and faeces are passed through the cloaca, which serves as the anus as well as the genitals and urinary duct [12]. Another species from the same genus as S. mokarran, the scalloped hammerhead (Sphyrna lewini), demonstrates an increased gastric evacuation rate with increased meal size [17], so this may be the case for S. mokarran as well. The amount of speculation I’m having to undergo for S. mokarran based off closely related species is evidence that S. mokarran needs more research and investigation to better understand it.

The small, relative size of the elasmobranch digestive tract may make room for the large liver. Baldridge (1970) found that the liver accounted for 3.83% and 9.5% of total body weight in two S. mokarran individuals (imagine a 100kg man having a 3.8 kg or 9.5 kg liver!!). Elasmobranchs do not have swim bladders like bony fish and instead rely on the liver, which is saturated in oil, to maintain buoyancy [19].  The liver contains lightweight oils, increasing its buoyancy and, along with its fins, gives it the lift it needs to prevent sinking.

Overall, not much is known about the reproductive biology of S. mokarran. Male specimens of S. mokarran have two claspers inside each pelvic fin [20] that deposit sperm into the female’s cloaca [21]. Based on evidence from other shark species, it is apparent that females can store sperm in their shell gland for up to 16 months [21]. S. mokarran are viviparous (birthing live young), and the ova has a yolk sac that, once depleted, turns into a structure similar to a placenta [1], [21]. They usually litter between 6–42 pups after a gestation of ~11 months [1], although one female was known to have littered a record 55 pups [22].

Lab 3

Specific objective:

  • Provide information about the age and growth of the specimen

The maximum reported age for S. mokarran is 30 years [1], although one specimen was estimated to be around 40–50 years old [22].

S. mokarran are the largest hammerhead species, and a male can reach a maximum total length (TL) of up to 610 cm, although typically, they will average 370 cm TL [1]. Due to their lack of otoliths, cartilaginous fish are aged by counting banding patterns on their sagittal vertebrae (Fig. 3). The von Bertalanffy growth function (VBGF) (Fig. 4) shows that, at birth, S. mokarran is around 50-70 cm.

Figure 3 Taken from [23]: “Sagittal vertebral section from a 4-year-old great hammerhead, Sphyrna mokarran, illustrating the banding pattern and annuli used to assign age. Scale bar = 2 mm.”
Figure 4 Taken from [23]: “The best fit von Bertalanffy growth model for male and female great hammerhead sharks, Sphyrna mokarran, collected in the northwestern Atlantic Ocean and the eastern Gulf of Mexico.”

The VBGF (Fig. 4) shows that males grow faster than females but reach a smaller asymptotic size than females. This growth is likely due to different energy requirements for the sexes for somatic growth and reproductive development [23].

S. mokarran reaches sexual maturity between 210–300 cm total length, with males tending to reach maturity at a smaller size than females [1].

Lab 4

Specific objective:

  • Provide information about the reproductive dynamics and life history of your chosen specimen

The embryonic sex ratio of S. mokarran is close to 1:1 [24]. It is gonochoric, with no interesting or outstanding sexual dynamics to note [1].

Rigby et al. (2019) describe S. mokarran as aplacental viviparous, whereas Froese and Pauly (2021) describe the species as viviparous with a yolk-sac placenta. Either way, they birth live young that have hatched from an egg in-utero.

There is not much research into the spawning behaviour of S. mokarran, which is perhaps reflective of their naturally elusive lifestyle. Stevens and Lyle (1989) note mating scars on females, which indicates, like many shark species, the courtship process can be seemingly violent with the male holding onto the females with his teeth during copulation.

S. lewini were observed in a large group off the Galapagos Islands and were thought to be amidst a courtship ritual where the largest females dominated the centre of the group, and the males attempted to access them to mate [26]. This could provide insight into the mating rituals of S. mokarran, although S. mokarran populations are substantially smaller than S. lewini, and they have yet to be observed in such large numbers.

One account of mating S. mokarran in the Bahamas reported two individuals ascending in 21m of water as they spiraled around one another and copulated at the surface [27].

S. mokarran birth between 6–42 pups every two years [25]. Their parental mode is not well researched. Many elasmobranchs offer no maternal care once the pup is born, so it can be assumed that this is the same for S. mokarran. However, a study on the scalloped hammerhead (S. lewini) and the Carolina hammerhead (S. gilberti) illustrated that neonatal hammerheads are likely to rely on maternal provisioning in the first few weeks after birth [28]. Therefore, an increased maternal investment may be a part of the life history strategy of S. mokarran. Again, further research is crucial to understand their reproductive and life histories further.

There is regional variation in the size and age range of S. mokarran sexual maturity. As before mentioned, this species reaches sexual maturity between 210–300 cm total length, with males maturing from 225–269 cm and females maturing from 210–300 cm [1], [25]. Age-at-maturity for females is estimated to be 5.5–8.3 years in Atlantic and Pacific populations [25], [29].

S. mokarran eggs hatch in-utero and embryonic individuals spend 11 months in their mother’s uterus, and newborns are around 50–70 cm total length and are then known as pups [25], [29]. At birth, they resemble S. mokarran adults in external morphology (Fig. 5). They grow rapidly until ten years of age, where their growth rate reduces [23], likely because they have reached sexual maturity and fitness rather than size becomes more critical for courtship and survival.

Figure 5 Neonatal great hammerhead, Sphyrna mokarran, pups. By Apex Predators Program, NOAA/NEFSC – http://nefsc.noaa.gov/rcb/photogallery/sharks/sharks.html, Public Domain, https://commons.wikimedia.org/w/index.php?curid=20004725

[1]      R. Froese and D. Pauly, “Sphyrna mokarran,” Fishbase, 2021. https://www.fishbase.se/summary/Sphyrna-mokarran.html (accessed Sep. 21, 2021).

[2]      V. Raoult, M. K. Broadhurst, V. M. Peddemors, J. E. Williamson, and T. F. Gaston, “Resource use of great hammerhead sharks (Sphyrna mokarran) off eastern Australia,” J. Fish Biol., vol. 95, no. 6, pp. 1430–1440, 2019, doi: 10.1111/jfb.14160.

[3]      D. D. Chapman and S. H. Gruber, “A further observation of the prey-handling behavior of the great hammerhead shark, Sphyrna mokarran: Predation upon the spotted eagle ray, Aetobatus narinari,” Bull. Mar. Sci., vol. 70, no. 3, pp. 947–952, 2002.

[4]      E. E. Josberger et al., “Proton conductivity in ampullae of Lorenzini jelly,” Sci. Adv., vol. 2, no. 5, pp. 1–7, 2016, doi: 10.1126/sciadv.1600112.

[5]      K. R. Mara, “Evolution of the Hammerhead Cephalofoil: Shape Change, Space Utilization, and Feeding Biomechanics in Hammerhead Sharks (Sphyrnidae),” University of South Florida, 2010.

[6]      S. M. Kajiura, J. B. Forni, and A. P. Summers, “Olfactory morphology of carcharhinid and sphyrnid sharks: Does the cephalofoil confer a sensory advantage?,” J. Morphol., vol. 264, no. 3, pp. 253–263, 2005, doi: 10.1002/jmor.10208.

[7]      W. R. Strong, F. F. Snelson, and S. H. Gruber, “Hammerhead Shark Predation on Stingrays: An Observation of Prey Handling by Sphyrna mokarran,” Copeia, vol. 1990, no. 3, p. 836, 1990, doi: 10.2307/1446449.

[8]      W. J. Vanderwright, J. S. Bigman, C. F. Elcombe, and N. K. Dulvy, “Gill slits provide a window into the respiratory physiology of sharks,” Conserv. Physiol., vol. 8, no. 1, pp. 1–10, 2020, doi: 10.1093/conphys/coaa102.

[9]      J. L. Dolce and C. D. Wilga, “Evolutionary and Ecological Relationships of Gill Slit Morphology in Extant Sharks,” Bull. Museum Comp. Zool., vol. 161, no. 3, p. 79, 2013, doi: 10.3099/mcz2.1.

[10]    P. J. Motta, “Prey Capture Behavior and Feeding Mechanics of Elasmobranchs,” in Biology of Sharks and Their Relatives, J. C. Carrier, J. A. Musick, and M. R. Heithaus, Eds. Boca Raton: CRC Press, 2004, pp. 165–202.

[11]    J. M. Brunnschweiler, P. L. R. Andrews, E. J. Southall, M. Pickering, and D. W. Sims, “Rapid voluntary stomach eversion in a free-living shark,” J. Mar. Biol. Assoc. United Kingdom, vol. 85, no. 5, pp. 1141–1144, 2005, doi: 10.1017/S0025315405012208.

[12]    S. C. Leigh, Y. Papastamatiou, and D. P. German, “The nutritional physiology of sharks,” Rev. Fish Biol. Fish., vol. 27, no. 3, pp. 561–585, 2017, doi: 10.1007/s11160-017-9481-2.

[13]    W. C. Hamlett, Sharks, skates, and rays: the biology of shark fishes. Baltimore: The Johns Hopkins University Press, 1999.

[14]    P. Jhaveri, Y. P. Papastamatiou, and D. P. German, “Comparative Biochemistry and Physiology , Part A Digestive enzyme activities in the guts of bonnethead sharks ( Sphyrna tiburo ) provide insight into their digestive strategy and evidence for microbial digestion in their hindguts,” Comp. Biochem. Physiol. Part A, vol. 189, pp. 76–83, 2015, doi: 10.1016/j.cbpa.2015.07.013.

[15]    R. D. Day, I. R. Tibbetts, and S. M. Secor, “Physiological responses to short-term fasting among herbivorous, omnivorous, and carnivorous fishes,” J. Comp. Physiol. B Biochem. Syst. Environ. Physiol., vol. 184, no. 4, pp. 497–512, 2014, doi: 10.1007/s00360-014-0813-4.

[16]    C. Bucking, “Feeding and Digestion in Elasmobranchs: Tying Diet and Physiology Together,” in Fish Physiology, vol. 34, Academic Press, 2015, pp. 347–394.

[17]    A. Bush and K. Holland, “Food limitation in a nursery area estimates of daily ration in juvenile scalloped hammerheads,” J. Exp. Biol. Ecol., vol. 278, pp. 157–178, 2002.

[18]    H. D. Baldridge, “Sinking Factors and Average Densities of Florida Sharks as Functions of Liver Buoyancy Published by : American Society of Ichthyologists and Herpetologists ( ASIH ) Stable URL : http://www.jstor.org/stable/1442317 REFERENCES Linked references are availabl,” Copeia, vol. 1970, no. 4, pp. 744–754, 1970.

[19]    M. Aidan, “Does Liver Size Limit Shark Body Size?,” Biology of Sharks and Rays, 2021. http://www.elasmo-research.org/education/topics/p_liver_size.htm (accessed Sep. 27, 2021).

[20]    M. Aidan, “Why Do Sharks Have Two Penises?,” Biology of Sharks and Rays, 2021. http://www.elasmo-research.org/education/topics/lh_2penises.htm (accessed Sep. 27, 2021).

[21]    M. Aidan, “From Here to Maternity,” Biology of Sharks and Rays, 2021. http://www.elasmo-research.org/education/topics/lh_maternity.htm (accessed Sep. 27, 2021).

[22]    “Record Hammerhead Pregnant With 55 Pups,” Discovery Channel, 2006. https://web.archive.org/web/20110622001318/http://dsc.discovery.com/news/2006/07/24/hammerhead_ani.html?category=earth&guid=20060724100030 (accessed Sep. 27, 2021).

[23]    A. N. Piercy, J. K. Carlson, and M. S. Passerotti, “Age and growth of the great hammerhead shark, Sphyrna mokarran, in the north-western Atlantic Ocean and Gulf of Mexico,” Mar. Freshw. Res., vol. 61, no. 9, pp. 992–998, 2010, doi: 10.1071/MF09227.

[24]    J. D. Stevens and J. M. Lyle, “Biology of three hammerhead sharks (Eusphyra blochii, sphyrna mokarran and s. lewini) from northern australia,” Mar. Freshw. Res., vol. 40, no. 2, pp. 46–129, 1989, doi: 10.1071/MF9890129.

[25]    C. L. Rigby et al., “Sphyrna mokarran, Great Hammerhead,” IUCN Red List Threat. Species, vol. e.T39386A2, p. 16, 2019, [Online]. Available: http://dx.doi.org/10.2305/IUCN.UK.2007.RLTS.T39386A10191938.en.

[26]    BBC Earth, “Hammerhead Sharks’ Complex Mating Rituals | BBC Earth,” 2019. https://www.youtube.com/watch?v=KsWuJtQpgsw (accessed Oct. 06, 2021).

[27]    “Great hammerhead shark – Sphyrna mokarran,” Shark Research Institute, 2021. https://www.sharks.org/great-hammerhead-shark-sphyrna-mokarran (accessed Sep. 27, 2021).

[28]    K. Lyons et al., “Maternal provisioning gives young-of-the-year Hammerheads a head start in early life,” Mar. Biol., vol. 167, no. 11, pp. 1–13, 2020, doi: 10.1007/s00227-020-03766-y.

[29]    H. H. Hsu et al., “Biological aspects of juvenile great hammerhead sharks Sphyrna mokarran from the Arabian Gulf,” Mar. Freshw. Res., vol. 72, no. 1, pp. 110–117, 2020, doi: 10.1071/MF19368.

An introduction to the thresher shark

Introduction

The thresher shark is an all-encompassing term referring to three surviving species from the family Alopiidae: the pelagic thresher (Alopias pelagicus), the bigeye thresher (Alopias superciliosus), and the common thresher (Alopias vulpinus).

Pelagic thresher shark (Alopias pelagicus). By Thomas Alexander – Own work, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=50280277
Bigeye thresher shark (Alopias superciliosus). By PIRO-NOAA Observer Program – http://ias.pifsc.noaa.gov/lds/obs_training/SharkThresherNew.pdf, Public Domain, https://commons.wikimedia.org/w/index.php?curid=6534429
Comparison between the three thresher species. By FactZoo.com – https://www.factzoo.com/fish/pelagic-thresher-shark-longtail-smack.html

Morphology

Thresher jaws are small. They have clearly not evolved to attack prey like tuna and seals; if anything, they look like they should be eating small crabs or scavenging chunks of floating debris that someone else took the time to kill. They would seemingly struggle to catch a live fish because the long snout overhangs their tiny mouth so much. That’s where the notorious tail comes in. The thresher tail is designed to be used like a whip to strike and immobilise prey [1], [2]. Such force occurs with a single tail slap that gas is diffused out of the seawater and rises to the surface in bubbles [1]. Typically, pelagic sharks hunt and capture one fish at a time; this strategy enables the shark to catch on average 3 fish, and sometimes more, in one go.

A sequence of still images taken from an overhead tail-slap hunting event [1].

The easiest way to differentiate between the three species is the colouration. Common threshers are likely to be more grey and they lack any colouration above their pectoral fins; sometimes, they have white dots on the tips of their fins. Pelagic threshers have distinct colouration above their pectoral fins. The bigeye’s eye is visible from the top of the head and has characteristic groves above the eyes and gills.

A common thresher shark, identified by the lack of colouration above the pectoral fin and white dots on the tips of the pectoral and dorsal fins. By Paul E Ester at English Wikipedia, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=19628266
A pelagic thresher shark, identified by the colouration above its pectoral fin. By NOAA Observer Program – http://www.fpir.noaa.gov/Graphics/OBS/obs_sharks/obs_pelagic_thresher_sharks/obs_pelagic_thresher_shark5.jpg, Public Domain, https://commons.wikimedia.org/w/index.php?curid=5553329
A bigeye thresher shark, distinguished by the birds-eye view of the large eyes and the lateral grooves. By PIRO-NOAA Observer Program – http://www.fpir.noaa.gov/Graphics/OBS/obs_sharks/obs_bigeye_thresher_sharks/obs_bigeye_thresher_shark5.jpg, Public Domain, https://commons.wikimedia.org/w/index.php?curid=6534392
A bigeye thresher shark is distinguished by its large eyes and lateral groove above the eye and gills. By PIRO-NOAA Observer Program – http://www.fpir.noaa.gov/Graphics/OBS/obs_sharks/obs_bigeye_thresher_sharks/obs_bigeye_thresher_shark4.jpg, Public Domain, https://commons.wikimedia.org/w/index.php?curid=6534388

Distribution

Threshers are pelagic, meaning they live in the deep, open ocean. The only thresher known to inhabit New Zealand waters is the largest of the trio, the common thresher [3]. The bigeye may also be found in NZ, but due to its habit of staying hundreds of metres below the ocean surface during the day, it is unlikely to be encountered if it is there at all [4].

Threats

The common and bigeye thresher are ‘Vulnerable’ to extinction under the IUCN Red List [3], [5], and the pelagic thresher is further threatened and classified as ‘Endangered’ [6]. Estimated global population reductions are as follows:

  • Common thresher: 30–49% over 3 generations (76.5 years)
  • Bigeye thresher: 30–49% over 3 generations (55.5 years)
  • Pelagic thresher: 50–79% over 3 generations (55.5 years)

All three species are globally targeted for their meat, fins, skin, and liver oil [7], the latter commonly used in modern cosmetics and supplements. All species are usually retained if accidentally caught on commercial vessels [8]–[11]. In one study [15] conducted in the Indian Ocean, 13 out of 19 bigeye threshers caught on a commercial vessel’s longline were dead upon retrieval. In the same study, in the Atlantic Ocean, 412 out of 849 bigeye threshers caught on longlines were dead. On the same ships were deaths of stingrays and manta rays as well as blue, shortfin mako, silky, and smooth hammerhead sharks. One of the largest hubs for shark fin trading globally is Hong Kong [9], and threshers accounted for up to 3% of the total fin mass in the past [8].

Threshers are also popular among recreational, big game anglers. Although a tag and release method is more commonly practised nowadays, there is also a risk of post-release mortality. With threshers likely to be hooked from their tail due to their hunting style, a study of common threshers found 78% of tail-hooked sharks died after release [12].

The New Zealand commercial fishery is not exempt from thresher shark landings. A recent report by Fisheries New Zealand [13] saw that in 5 years from the 2014/15 to 2018/19 commercial fishing seasons, 149,916 tonnes of common thresher shark were caught by the core deep-water fleet. With the average 5-metre common thresher shark usually weighing in at 230 kg, we can infer that in the 5 years, the deep-water fleet landed approximately 651 individual thresher sharks.

Thresher vs swordfish

In April 2020, a dead, 4.5 metre, female bigeye thresher was found beached on a Libyan coast [14]. A 30 cm swordfish (Xiphias gladius) rostrum was found embedded in its head. It is understood that the rostrum severely injured some of the shark’s nerves, arteries, and gill arches. It was concluded that the impalement was what led to the ultimate death of the shark.

A young swordfish (Xiphias gladius). By Michael Landress, CC BY-NC-ND 2.0https://www.flickr.com/photos/myfwc/26802909040
Taken from Jambura et al (2021) [14]. “Female bigeye thresher Alopias superciliosus (TL = 445 cm) stranded on the Libyan coast (Mediterranean Sea), with a swordfish Xiphias gladius rostrum embedded deep in the branchial chamber. Scale bars indicate 50 cm (b) and 10 cm (c and d). Photo (a and b) and video content (c and d) courtesy of Faraj Habrisha and Abdalhakim Ahmed Al sebaihe”.

[1]        S. P. Oliver, J. R. Turner, K. Gann, M. Silvosa, and T. D’Urban Jackson, “Thresher Sharks Use Tail-Slaps as a Hunting Strategy,” PLoS One, vol. 8, no. 7, 2013, doi: 10.1371/journal.pone.0067380.

[2]        S. A. Aalbers, D. Bernal, and C. A. Sepulveda, “The functional role of the caudal fin in the feeding ecology of the common thresher shark Alopias vulpinus,” J. Fish Biol., vol. 76, no. 7, pp. 1863–1868, 2010, doi: 10.1111/j.1095-8649.2010.02616.x.

[3]        C. L. Rigby et al., “Alopias vulpinus,” IUCN Red List Threat. Species 2019, vol. e.T39339A2, 2019.

[4]        H. Nakano, H. Matsunaga, H. Okamoto, and M. Okazaki, “Acoustic tracking of bigeye thresher shark Alopias superciliosus in the eastern Pacific Ocean,” Mar. Ecol. Prog. Ser., vol. 265, pp. 255–261, 2003, doi: 10.3354/meps265255.

[5]        C. L. Rigby et al., “Alopias superciliosus,” IUCN Red List Threat. Species 2019, vol. e.T161696A, 2019.

[6]        C. L. Rigby et al., “Alopias pelagicus,” IUCN Red List Threat. Species 2019, vol. e.T161597A, 2019, doi: https://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS.T161597A68607857.en.

[7]        R. W. Jabado et al., “The trade in sharks and their products in the United Arab Emirates,” Biol. Conserv., vol. 181, pp. 190–198, 2015, doi: 10.1016/j.biocon.2014.10.032.

[8]        S. C. Clarke, J. E. Magnussen, D. L. Abercrombie, M. K. McAllister, and M. S. Shivji, “Identification of shark species composition and proportion in the Hong Kong shark fin market based on molecular genetics and trade records,” Conserv. Biol., vol. 20, no. 1, pp. 201–211, 2006, doi: 10.1111/j.1523-1739.2005.00247.x.

[9]        A. T. Fields et al., “Species composition of the international shark fin trade assessed through a retail-market survey in Hong Kong,” Conserv. Biol., vol. 32, no. 2, pp. 376–389, 2018, doi: 10.1111/cobi.13043.

[10]      S. C. Clarke et al., “Global estimates of shark catches using trade records from commercial markets,” Ecol. Lett., vol. 9, no. 10, pp. 1115–1126, 2006, doi: 10.1111/j.1461-0248.2006.00968.x.

[11]      F. Dent and S. Clarke, “State of the global market for shark products,” Rome, Italy, 2015.

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Estuaries: how habitats and food webs create transitional estuarine ecosystems of high productivity

Introduction

An estuary is a coastal passage of water where tides from the open sea meet river currents, and salty seawater mixes with fresh riverine water to create an environment of high productivity (Correll, 1978; Pritchard, 1967). The intermediate location of estuaries causes it to act as a transitional environment between terrestrial and marine ecosystems. Estuaries can be viewed as a continuum, whereby further upstream, the calmer, fresher water of the river progresses into the tidal, saline water of the ocean. This estuarine continuum – due to the range of its attributes, including salt content, depth, temperature, tidal energy, et cetera – allows for the diversification of the habitats within it. Three key estuarine habitats include salt marshes, mangroves, and seagrass beds. The organisms within these habitats interact with one another in numerous ways, creating not only food chains but food webs of complex interactions and energy exchanges.

Correll (1978) states that estuaries are areas of unusually high productivity because the conditions that create estuaries result in high levels of photosynthate from in situ primary production byphytoplankton and plants. Estuarine food webs are sustained by their habitats; therefore, it is important to analyse the relationship between habitats and food webs and how they contribute to the overall high productivity of estuaries. Furthermore, because estuaries are closely linked with terrestrial and marine ecosystems, estuarine productivity may be attributed to or contribute to adjacent environments.

In this essay, I will do the following: describe the features of estuarine habitats and food webs; determine how estuarine habitats and food webs are both linked with terrestrial and marine ecosystems, making estuaries a transitional environment; and critically analyse how habitats and food webs contribute to a highly productive estuarine system.

Estuarine habitats

In order to analyse the high productivity of estuaries, it is crucial first to explain the features of estuarine habitats and the organisms which inhabit them. Links to food webs from the habitats can then be made to understand better how energy and nutrients enters the estuarine system. Three important estuarine habitats exist, including salt marshes, mangroves, and seagrass beds; each possesses unique attributes and organisms living there.

Salt marshes are wetlands dominated by few species of halophytic vegetation and are alternately inundated and drained by the tides (Christiansen, Wiberg, & Milligan, 2000; Gedan, Altieri, & Bertness, 2011; Richardson, Swain, & Wong, 1997). The halophytic plants add stability to the marsh by trapping and binding sediment and can also withstand stressful conditions like the constant flooding and draining of the marsh as well as the salty, waterlogged, and, sometimes, hypoxic soil (Gedan et al., 2011; Pennings, Grant, & Bertness, 2005). Three types of fauna utilise the salt marsh habitat. (1) Specialist species inhabit marshes as their primary home, utilise the high vegetation biomass for energy, and are well adapted against desiccation; these specialist animals tend to be invertebrate species (Kon et al., 2012; Minello & Webb, 1997; Richardson et al., 1997). (2) Another type of fauna uses marshes as an extension of their home and are therefore regular visitors to the marsh. As a general example, a crab species uses the marsh for protection while their home in the mudflat is under heavy predation, then returns home once predation has eased. (3) Terrestrial or ariel species venture into the marsh for certain activities such as gathering food, courtship, or nesting (Burger, 1979; Hanson & Shriver, 2006; Teixeira, Duarte, & Caçador, 2014). Overall, the conditions that define a salt marsh create a habitat dominated by marine invertebrates (Daiber, 1982).

Restored Tomago salt marsh #marineexplorer | Coastal salt ma… | Flickr
Restored Tomago salt marsh.
By John Turnbull – Own Work, CC BY-NC-SA 2.0, https://www.flickr.com/photos/johnwturnbull/31538875578/

Mangroves are woody plants that can withstand excessive salt concentrations and water inundation, and “true” mangroves are from the genus Rhizophora. Mangroves are distributed globally in tropical and sub-tropical regions (Parida & Jha, 2010; Simard et al., 2019). Mangrove plants contend with adverse conditions like saline water and anoxic substrates, which are difficult, if not impossible, environments for terrestrial plants to live in. Mangroves have combatted this by developing salt glands, roots with low permeability, and adventitious roots with pneumatophores (Liang, Zhou, Dong, Shi, 2008; Medina, 1999; Parida & Jha, 2010; Yáñez-Espinosa, Terrazas, & Angeles, 2008). The foliage, trunks, and roots of mangroves all provide unique niches for organisms to inhabit (Nagelkerken et al., 2008). Above the water, the foliage provides a habitat for terrestrial fauna like birds, mammals, reptiles, and insects. The trunks and pneumatophores provide a rigid substrate for organisms to settle on. Under the water, the roots can support sponges, bivalves, and algae, and provide a labyrinth of microhabitats for aquatic species like fish. Due to the abundance of food and shelter, mangroves may function as a nursery for juvenile fish and invertebrates species (Nagelkerken et al., 2008).

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Mangrove roots.
By Jonathan Wilkins – Own work, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=40213291
Above and below water view of mangroves and roots.
Public Domain, https://commons.wikimedia.org/w/index.php?curid=142126

Seagrasses are the only flowering plants that have evolved to survive submersion in saltwater (Orth et al., 2006). The seagrasses, anchored to the sediment by underground runners called rhizomes, congregate to form vast beds that provide a large habitat area for organisms to inhabit. The stability of seagrass habitats means it is a popular environment for transient species to lay eggs and is one of the most productive and diverse marine ecosystems (Constanza et al., 1997; Duarte & Chiscano, 1999). Seagrass habitats provide shelter, food, and a nursery area for fish and marine invertebrates as well as food for waterfowl and marine mammals like dugongs and manatees (Heck, Hays, & Orth, 2003; Holm & Clausen, 2006; Rybick & Landwehr, 2007; Thayer, Bjorndal, Ogden, Williams, & Zieman, 1984; Weisner, Strand, & Sandsten, 1997).

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Seagrass meadow (Zostera marina) in the Dzharylhach Bay, Ukraine.
By Sofia Sadogurska – Own work, CC BY 4.0, https://commons.wikimedia.org/w/index.php?curid=97165229
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Carbon uptake and photosynthesis in a seagrass meadow. Special cells within the seagrass, called chloroplasts, use energy from the sun to convert carbon dioxide and water into carbohydrates (or sugar) and oxygen through photosynthesis. Seagrass roots and rhizomes absorb and store nutrients and help to anchor the seagrass plants in place.
By Cullen-Unsworth L, Jones B, Lilley R and Unsworth R – [1], CC BY 4.0, https://commons.wikimedia.org/w/index.php?curid=89279174

Estuarine food webs

Habitats contain niches that make way for a variety of interactions between organisms. In estuaries, salt marshes, mangroves, and seagrass beds create unique environments that induce complex food webs. These food webs begin with an input to the first trophic group known as the primary producers, a group that includes phytoplankton or plants like the vegetation of salt marshes, algae, and seagrasses. Trophic transfers take place from one group to another as the energy that began with primary production is moved up the food web to other trophic groups like herbivores or carnivores. During trophic transfers, some energy may be transported out of the food web into a cycle (such as the nitrogen cycle) or be expelled as a respiratory end product (Day, Kemp, Yáñez-Arancibia, & Crump, 2012).

File:FoodWeb.svg
A freshwater, marine, and terrestrial food web.
By File:FoodWeb.jpg: Thompsmaderivative work: Pixelsquid – This file was derived from: FoodWeb.jpg:, CC0, https://commons.wikimedia.org/w/index.php?curid=102527971

Detritus is dead, particulate, organic material, and can be processed repeatedly by organisms at most levels of a food web until it is either buried in sediment or exported (Darnell, 1961); therefore, detritus is an important input to food webs. Salt marsh vegetation, mangrove litter, and seagrasses are likely to provide significant amounts of plant detritus to estuarine ecosystems (Teal, 1962; Odum & de la Cruz, 1963).

Estuaries as transitional environments of high productivity

Estuaries are a transitional environment between terrestrial and marine ecosystems. Terrestrial species will use estuarine salt marshes for specific activities because the marshes provide an environment unlike any terrestrial habitat. Furthermore, fishes may also enter salt marshes at high tide to feed before returning to the marine environment (Heck et al., 2008). Liang et al. (2008) determined mangroves as a buffer for the terrestrial environment against marine energies such as erosion and damage from waves and typhoons. Seagrasses provide an essential link from estuaries to marine ecosystems because live seagrass leaves not consumed enter the detrital pool (Heck et al., 2008). The detrital seagrass can be transported by currents and waves over extensive distances and be used by organisms for shelter, habitat, or consumed along the way (Ochieng & Erftemeijer, 1999; Thresher, Nichols, Gunn, Bruce, & Furlani, 1992). The detrital seagrasses journey may conclude in deep-sea canyons, where it accumulates and supports organisms in an environment with poor habitat structure and low primary production (Josselyn et al., 1983; Vetter, 1998). Thus, seagrass meadows link estuaries with an unlikely marine environment, the deep sea.  Estuaries also receive significant detritus inputs from both terrestrial and marine ecosystems (Day et al., 2012).

Estuaries are thought to be highly productive per unit area. This high productivity can mean that the plants are very productive, that more organic matter is produced than used, or that estuaries sustain a substantial amount of fauna compared to other environments (Day et al., 2012). Schelske and Odum (1962) considered the different contributors to one estuary’s productivity, and these can be extended to all estuaries in a general sense:

  • Firstly, there is diversity in the sources of organic matter that enter an estuary. The three key estuarine habitats (salt marshes, mangroves, and seagrass beds) all provide organic matter to estuarine systems. These habitats provide substrata for epiphytic algae to grow on and shallow, photic waters for pelagic phytoplankton. Adjacent terrestrial environments also passively contribute organic matter into the estuarine system. More specifically, the many sources of organic matter in an estuary can be narrowed down to a diverse species abundance of photosynthetic organisms. This means that light can be utilised throughout all seasons, reducing the chance of a substantial drop in organic matter production by the photosynthesising species.
  • Secondly, physical energy, such as tides, currents, wind, and waves, produces considerable water movement in estuarine ecosystems, increasing the surface area by which phytoplanktonic photosynthesis can occur. For example, the flooding and draining of a salt marsh transports material and nutrients in and out of the marsh, and tides and currents transport unused seagrasses out of the seagrass beds to enter a different part of the food web.
  • Thirdly, an abundant supply of various nutrients is thought to be present in estuaries, especially when compared to marine and freshwater environments. Nutrient abundance in estuaries allows for a higher rate of photosynthesis (Nixon 1980, 1995; Rhyther & Dunstan, 1971).
  • Finally, because estuaries are relatively shallow and well-mixed, both food and nutrients are available to all organisms in the water column and benthic and pelagic food webs can be coupled, creating interactions that may be unique to estuaries alone (Day et al., 2012). Bivalves and microorganisms also play a role in biogeochemical cycling of nutrients. The mixing of salt and freshwater provides high nutrients in both the water and the sediment.

Habitats could potentially be viewed as the most important contributor to estuarine productivity because they give way to the environments which allow estuaries to be productive; the complexities of estuarine food webs would cease to exist if it were not for the availability of diverse habitats in which they can operate. Salt marsh, mangrove, and seagrass bed ecosystems have relationships with terrestrial and marine ecosystems, increasing estuaries’ productivity. The value of these habitats to certain trophic levels depends on their needs for shelter, food, or to carry out species-specific activities, showing that the way these habitats are structured affects trophic transfers in estuarine food webs (Walters, 2000). Some estuarine habitats may increase production in other estuarine habitats and adjacent ecosystems. The diversity of the mangrove ecosystems gives way to a rich microbial community, supported by nutrient cycling, which may promote faster sponge growth than in coral reefs (Kathiresan & Bingham, 2001). Odum and Helad (1972) suggest that the production of mangroves is exported to the marine environment, which provides food for secondary consumers and may lead to higher production in the marine ecosystem. Heck et al. (2008) describes how the highly productive nature of seagrass meadows can spill over into other ecosystems. For example, some fish live in mangroves but feed on seagrass, creating a trophic link between the two habitats. Also, some fish that inhabit coral reefs feed on seagrass, shifting organic matter and nutrients into the reef habitat and food web.

Conclusion

Productivity of any ecosystem is easily measured by the quantity of photosynthate it can produce because primary production essentially supports entire food chains. Estuaries have such a plethora of trophic interactions that it is necessary to extend their food chain to a food web that spans multiple ecosystems. This food web would cease to exist without the dynamic habitats that support them, with the key habitats being salt marshes, seagrass beds, and mangroves. The features that make these habitats unique from any other habitat globally, are also the features that sustain the species that live in them. Because estuaries are a transitional environment between terrestrial and marine ecosystems, it is likely that they benefit from the high productivity of estuaries, and this may be shown through the trophic interactions and nutrient cycling that occurs. Estuaries are a dynamic environment, and further research is needed to understand the global effect of their high productivity to learn how to better protect them.

Reducing pressure on Auckland's estuaries
An estuary in Auckland, New Zealand, showing how closely estuaries and terrestrial (specifically urban) environments are linked.
By Getty Images, https://www.newsroom.co.nz/ideasroom/reducing-pressure-on-aucklands-estuaries

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The species-area relationship and Bergmann’s rule: attempts to explain global patterns in biodiversity

Introduction

Humans have noticed the differences between species worldwide from the time they evolved up until the present, with the term “biodiversity” first being used by Tangley (1985). A natural progression from these discoveries of global biodiversity was to explain them using such rules as the species-area relationship (SAR) and Bergmann’s rule. SARs describe the link between the area of a habitat and the number of species found within that area (Losos & Schulter, 2000; Preston, 1962). Bergmann’s rule states that species of larger size are found in colder regions, and species of smaller size are found in warmer regions (Ashton, Tracey, & de Queiroz, 2000; Mayr, 1956). Both rules are utilised in the field of biogeography, and I will be looking at evidence that both supports and opposes SARs and Bergmann’s rule to critique the validity of each.

The SAR model has ideas such as island biogeography theory (IBT) and spatial scales and studies that support it as an ecological law (Franzén, Scweiger, & Betzholtz, 2012; Losos, 1996; Losos & Schluter, 2000; Rand, 1969). IBT states that larger islands have greater numbers of species than smaller islands (MacArthur & Wilson, 2001; MacGuinness, 1984) and spatial scales keeps each SAR study relevant to the size at which the study was undertaken (Drakare, Lennon, & Hillebrand, 2006; Turner, 2005; Tylianakis, Klein, Lozada, & Tscharntke, 2006). Criticism of IBT says that its equilibrium theory is too simplistic, which raises questions about it being successfully used to support SARs (Heaney, 2000; Lomolino, 2000; Tangney, Wilson, & Mark, 1990; Toft & Schoener, 1983; Webb & Vermaat, 1990; Wu, 1995). A lack of real-life SAR studies poses the question: is SARs more valuable as a tool for biogeography rather than an ecological rule (Diamond, 1984; Zimmerman, 2000)? 

Bergmann’s rule is supported by real-life studies that not only expressed the rule but followed a logical reason as to why they adhered to it (Ashton, Tracy, & de Queiroz, 2000; Fujita, 1986; Gigliotti et al., 2019; James, 1983; Rhymer, 1992; Sand, Cederlund, & Danell, 1995; Weaver & Ingram, 1969). Conversely, there are some exceptions to Bergmann’s rule that also carry their own rational explanation (Gigliotti et al., 2019; Oishi, 2010; Takeuchi, 1995; Kaneko, 1988). Geist (1987, 1990) disagrees with Bergmann’s rule and pointed out that not only is body mass a poor conserver of heat, but that body size is also due to a multitude of different factors. 

Species-area relationship

Supportive evidence for species-area relationship

SARs depict the number of species found in an area of habitat and are plotted on a graph to show a species-area curve where x = habitat area and y = species richness (Rosenzweig, 1995). The typical outcome of plotting SARs on a graph is a sharp increase in species richness over the initial area that begins to taper off as distance increases; it shows that, over a habitat area, species richness increases. Franzén et al. (2012) regarded SARs as an ecological tool used to make predictions for areas that have little or no data behind them. This means SAR predictions can be used as a powerful instrument in conservation for remote habitats or when there is little time to collect data in the field. 

The theory of island biogeography was coined by MacArthur and Wilson in 1967, and it states that species richness increases with island size and decreases with island distance from the mainland (MacArthur & Wilson, 2001). These islands receive new colonising species from the mainland, and, eventually, established populations of species become extinct; this creates an equilibrium point where immigration equals extinction. A study by Riebesell (1982) found that the species richness of plants on 13 peaks in the Adirondack Mountains is due to the area of the alpine ecosystem and immigration between summits. This reflects IBT as the plant seeds have been spread by birds and dropped on mountaintops (more seeds dropped on a bigger area). Extinction was evident because the plants on the island were not genetically identified as relict populations, meaning that an equilibrium has been met between seed dispersal (immigration) and plants dying (extinction). 

Spatial scales are essential in verifying the use of SARs in the context of the study being undertaken (C. Bishop, personal communications, May 7, 2020). This amplifies SAR effectiveness because it gives a guideline as to how SARs should be studied and therefore reduces the likelihood of error; when spatial scales are considered during SAR research, it increases the integrity of the research. Turner and Tjørve (2005) discuss spatial bias, where smaller areas are likely to be surveyed more intensely than larger ones for practical reasons, meaning that the number of species being sampled can potentially decrease with an increase in area. In a scenario such as this, the data will less likely represent the actual species richness of the area, reducing the validity of the species-area rule. A study of anthropogenic influences on bees and wasps by Tylianakis et al. (2006) found that estimation of species diversity of a larger area based on evidence gathered at a smaller spatial scale underestimated the actual result; had this gone unnoticed, it would have meant that greater conservation attention would have been given to the wrong area. This verifies the importance of using spatial scales to enhance SARs’ effectiveness.

Studies, such as those undertaken by Losos (1996) of the Anolis lizard and Franzén et al. (2012) of butterflies and moths on true islands show SARs as real examples. Losos (1996) found in his study of Anolis lizards on 147 Caribbean islands that a significant relationship exists between the number of species and area of the island. Larger islands were found to have more species present than smaller islands that were more geographically isolated and did not support more than 2 Anolis species at a time. This supports IBT and shows that Anolis lizards on smaller, more isolated islands have reached an equilibrium point, such as the one discussed by MacArthur and Wilson (2001). A positive relationship between area and species richness of 1016 moth and butterfly species was recorded by Franzén et al. (2012), who also noted species with a smaller geographic range were more sensitive to area change than species with a larger range; this emphasises the importance of spatial scales within SAR studies.

Counter-evidence for species-area relationship

There is a discussion about MacArthur and Wilson’s (2001) IBT to be used as more of a framework than a theory. It needs to be modernised, especially as its equilibrium model appears too simplistic (Heaney, 2000; Lomolino, 2000). As IBT is a SAR, any fragility found within IBT raises questions about the reliability of SARs as a law. IBT’s equilibrium model’s simplicity lies in the fact that it only accounts for species richness due to immigration and extinction and no other factors. Even so, the idea of equilibrium being reached on an island seems far-fetched as ecological stochasticity and geographical and geological fluctuations can affect a perfectly balanced model. Tangney et al. (1990) listed five other possible explanations for any studies that showed results consistent with IBT. These include random placement hypothesis (Arrhenius, 1921), habitat diversity hypothesis (Williams, 1943), incidence function hypothesis (Diamond, 1975), small island effect hypothesis (Whitehead & Jones, 1969), and small island habitat hypothesis (Kelly, Wilson, & Mark, 1989).

Assumptions of IBT (MacArthur & Wilson, 2001), and therefore SARs, can be challenged:

  1. Species richness balances immigration rates and extinction rates, excluding speciation over evolutionary time. For example, the adaptive radiation resulting in different finch species on the Galapagos Islands (Grant & Grant, 2008).
  2. The assumption that immigration rates to an island result from island size and distance from the mainland fail to account for other variables. These variables include the role ocean and air currents play in transporting species to islands (Payn, Dvorak, & Myburg, 2007), anthropogenic introduction of species, or immigration from other islands or emigration from the island.
  3. IBT ignores stochastic events and assumes that all species have an equal ability to immigrate or become extinct.
  4. Natural disasters can cause extinction on islands; natural disasters can also function independently of island size or distance to the mainland. 
  5. Climate can affect the species’ likelihood to immigrate to or leave an island. For example, a species that functions in colder weather on the mainland is unlikely to leave its niche to travel to a warmer island, and vice versa, regardless of the islands size or proximity to the mainland.

As mentioned before, SAR’s equations and models are used in conservation. Still, Zimmerman and Bierregaard (1986) introduce the thought of SAR data acting as a “blindman’s cane [to] show us roughly the way” (p. 141) after stating that predictions using IBT and SARs for conservation were nonbeneficial. Diamond (1984) mentions that the speed at which environments are being dismantled should cause ecologists to erect conservation plans faster for them to be preserved. A study of Amazonian frog conservation (Zimmerman and Bierregaard, 1986) was used as a case for the misuse of SARs and IBT and showed that these models may underestimate species richness. Therefore, mean areas receive less conservation than they need. Zimmerman and Bierregaard (1986) propose that time spent studying theory would be better used to understand the relationships that species have with their environment, which would, in turn, produce a better estimate of species richness in an area than using SAR equations. There were many articles available on SARs, yet it was all theory with little in-field evidence; lack of evidence challenges the integrity of the law. The questions here are: is the SAR model an excuse to use maths and models instead of physical evidence which could say otherwise? Is there too much theory and not enough tested hypotheses? Is the consequence of a lack of conservation, where it is needed, taxonomic extinction? In-field experimentation is necessary to answer these questions.

Bergmann’s rule

Supportive evidence for Bergmann’s rule

Bergmann’s rule says species of larger size are found in colder environments, whilst their smaller counterparts are found in warmer environments (Ashton, Tracey, & de Queiroz, 2000; Mayr, 1956). Many arguments have arisen about the validity of Bergmann’s rule (Geist, 1987, 1991; Paterson, 1990), yet, animals are not set aside from the laws of physics (Cambell, 1977), and Paterson (1988) states that Bergmann’s rule obeys mass and surface-area heat-transfer rules. (It is important to note that this refers to their mass or surface area when referring to smaller and larger individuals, rather than length unless noted (Paterson, 1988).)

Evidence of geographic variation in body size of birds has a solid environmental link, including that of the mallard ducks (Anas platyrhynchos) of America and Canada (Rhymer, 1992). It was found that the growth of the mallard ducklings was constrained by environmental conditions experienced during development; tarsus length was 3% longer in the colder Canadian population, and it was shown that this variation was due to the environment they were exposed to during maturation. James (1983) conducted a study with 12 avian species in the central and eastern United States. He found intraspecific size variation is related to a combination of temperature, moisture, and other climatic variables, rather than just temperate ones. A modification of Bergmann’s rule to include this will maintain the integrity and framework of the rule whilst adding more information and specificity to it.

Mammals in both controlled and natural environments displayed evidence of adhering to Bergmann’s rule. Pigs (Sus scrofa domesticus) raised at 5oC were bigger than pigs of the same species raised at 35oC (Weaver & Ingram, 1969). Swedish moose (Alces alces) not only had a 15-20% larger body mass in colder, northern areas than in the south, but also had higher growth rates and matured later than in warmer areas (Sand et al., 1995), indicating a slower metabolic rate for moose in colder environments. Bats (Myotic lucifugus) also showed a similar metabolic correlation to latitude and conforming to Bergmann’s rule in that the colder population grew slower, showed delayed aviation development, and were born larger (Fujita, 1986).

Northern American populations of snowshoe hare (Lepus americanus) conform to Bergmann’s rule to mitigate heat loss (Gigliotti et al., 2019). They can withstand the colder winter months by conserving heat and energy due to increased body mass. The strong selection pressure for larger female snowshoe hares is because females have higher energy demands due to gestation and lactation; the hares breed in winter months, so conserving energy during the cold period whilst also having maternal demands is essential for the hare. 

Counter evidence for Bergmann’s rule 

Contrarily, southern American snowshoe hare populations do not follow Bergmann’s rule as strongly as their northern counterparts (Gigliotti et al., 2019). This is an example of different selection forces acting on individuals, even within a species. In the northern population, a big driver for body mass was to conserve energy and mitigate heat loss, whilst, in the southern population, their large body mass was a result of an extended growing season. Gigliotti et al. (2019) found that the milder, southern winter meant heat conservation wasn’t an essential factor in determining hare body mass. Furthermore, southern populations experienced a long summer growing season and a shorter winter, meaning they had more time to accumulate body mass and less time to lose it.

Two subspecies of red fox (Vulpes vulpes) in Japan show a negative correlation to Bergmann’s rule as skull size is bigger in the subspecies inhabiting the warmer, southern regions than the subspecies inhabiting the colder, northern region (Oishi, 2010; Takeuchi, 1995). Oishi (2010) found the southern subspecies showed increasing skull size with decreasing latitude across its populations. Although the body length of the northern subspecies was larger than the southern subspecies, the male body weight was the same between both, and the female body weight was lighter in the northern species, countering Bergmann’s rule as colder populations had less body mass.

Geist (1987, 1990) opposes Bergmann’s rule with solid reasoning. Firstly, because Bergmann’s (1847) article is written in German, translation has become an issue, with many people following Mayr’s (1956) translation, which Geist (1989) claims is wrong. Secondly, using formulas derived from Bergmann’s rule, Geist (1987, 1990) predicts an exponential size increase with latitude, anticipating higher latitudinal populations of Calgarian sparrows to be the size of chickens, which they are not. Thirdly, Geist (1987) concludes that hair is a superior adaption than size to cold, predicting a hairless beast at different temperate intervals would finally have to weigh 15,000kg at a temperature of –32oC, whereas, for the same beast, 1cm of hair coat is worth a 5-fold increase in mass. Consequently, if it is cheaper to evolve a denser coat, evolution would favour this over body mass increase when subjected to cold stress. Finally, Geist (1990) concludes that body size depends not only on heat retention but also on other factors. These include: individuals surviving longer on larger fat stores; larger females bearing more and producing larger young; larger females producer richer or more milk, therefore sustaining healthier or more young respectively; large size favouring males in fighting and sexual selection; larger individuals can run for more extended periods (helpful in prey species were speed and endurance are necessary for survival). When considering these, it seems far-fetched that body size is solely due to selection for heat conservation at any latitude.    

Significance of ideas

In biogeography, it is essential to scrutinise these rules because it not only helps argue their place in science but uncovers more and more about the distribution of species in space and time. For SARs, it seems that more real-life evidence is needed to properly analyse this rule. For now, caution should be exercised when using it as a conservation tool. For Bergmann’s rule, it is clear there is a difference between and amongst species of different latitudes. Yet, it is naive and bold to assume these differences come down to something as simple as energy conservation. It seems far-fetched that Bergmann’s rule will hold true to species worldwide when you take in the complexities and specialised adaptations of the natural world.

I believe it is a scientist’s job to doubt rules (if only to end up strengthening their integrity in the end). Both SARs and Bergmann’s rule are a stepping-stone to the truth that nature hides. Any disparities should be indications of necessary modifications rather than a chance to disregard the rule entirely. 


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Rarotonga

What do you do when you’ve just finished a stressful semester at uni, and your tenancy application for a new house has been accepted? You ditch New Zealand and head to Rarotonga for 2 weeks! With the quarantine-free travel bubble opening between NZ and the Cook Islands and flights and accommodation being ridiculously affordable, trading in Auckland’s sub-zero temperatures for a tropical paradise seemed to be the only reasonable choice.

The climate was the first thing that got me about Raro. Snapchat was covered with 7am stories of frost-covered grass, and I’m getting a sweat on just walking to breakfast. I think the next thing I quickly noticed was the atmosphere. It’s a small island (67 km2; a population of 13,000), and the convivial ambience of the community was almost tangible. The way the bus driver greeted me, you’d think he was my uncle. After being in Raro for only a day, I felt the same feeling of being in Pukekohe; I felt like I was home.

Snorkelling

Obviously, the daily routine began with breakfast. Then, as soon as we could get our shit together, we went snorkelling. The water was so warm and so salty. One of the locals said that as kids, they all swam in the ocean with their eyes open to get used to the salt. I totally understand why they did that because water leaked into my mask one time and I thought I went blind. In NZ, in the height of summer, I can rarely go freediving in just a bikini for more than 30 minutes before the cold sets in; in Raro, I almost felt too hot when I was snorkelling in my 3 ml spring suit – crazy. The ocean would probably feel like a bath in summertime.

To me, the most interesting animal I saw while snorkelling in the lagoon was the octopuses. I feel like every time I go freediving and there’s an octopus, everyone but me manages to see it; not this time, suckers (pun intended). They inhabited the right-hand side of the lagoon, amongst an area of littered stones and rubble. They were day octopuses (Octopus cyanea) who, unlike their nocturnal counterparts, are active during the day, stealthily patrolling the reef under an impressive camouflage [1, 2]. One of them even attempted to steal my GoPro and take it into its den for further inspection.

Bluefin trevally (Caranx melampygus) are the top predators in the Rarotongan lagoon systems. I came across a school of them. When I first saw one of them in the distance, I honestly thought it was a juvenile reef shark trapped in the lagoon. Once I got closer and noticed more of them, I realised they were, unmistakeably, trevally. They outsized all the other reef fish by three-fold, and they proved their predator status as they confidently cruised past me at arms-length. The biggest members of this school appeared to be around 70cm, putting them at the age of approximately 8 years [3].

Moray eels would appear out of nowhere in crevices and holes in the reef. Sometimes, I’d sink to the sand on my knees to be face to face with them for a moment and appreciate their beautiful ugliness and imagine what it’s like to be a little fish caught in their pharyngeal jaws.

The coral was beautiful, and, like the octopus, I have never seen coral like that in the wild before. The variation in size and colour was magnificent. So was the fact that they live in a highly changing, intertidal environment; I couldn’t touch the sandy bottom at high tide compared to the exposed reef at dead low. There was an abundance of brain coral and table coral, as well as soft coral species.

Darting around were parrotfish, doing their crucial job of scraping and cleaning the coral to keep it healthy.

The coral themselves provide homes for thousands of reef fish and act as a barrier for incoming waves that intend to reach the island. It is said that even though coral reefs cover less than 1% of the ocean floor, they provide support for around 25% of all known marine species.

Burrowing urchin (Echinometra mathaei)
Lionfish (Pterois sp.)
Threadfin butterflyfish (Chaetodon auriga) and black triggerfish (Melichthys niger)
Giant clam (Tridacna sp.)
Starry pufferfish (Arothron stellatus)
Peacock grouper (Cephalopholis argus)
Giant clam (Tridacna sp.)
Mushroom coral (Fungiidae sp.)

This environment was like nothing I had ever seen before. I wanted to spend every moment under that water; if a genie granted me only one wish, it would be to breathe underwater. Then again, my wish partly comes true every time I strap on some SCUBA gear and descend down 5 metres, 10 metres, 20 metres… which is exactly what I did.

Diving

Our first dive was the Papua Passage. Literally, a passage between two tall cliffs that felt like I was doing some sort of underwater, horizontal rock climbing to pass through. But, oh boy, was it worth it. Turtles everywhere you looked, sleeping on coral, drifting lazily past with their heavy eyes watching you meticulously. Two species exist in the Cook Islands, the endangered green turtle (Chelonia mydas) [4] and the critically endangered hawksbill turtle (Eretmochelys imbricata) [5], and I had the pleasure of meeting both.

Look closely at that photo. You can see the rear right quarter appears to be missing. If I had to take a guess, and I’ve stared at this photo forever trying to decipher it, then I would say that a shark, most likely a tiger, managed to get itself a quick on-the-go snack. This turtle is living proof that what doesn’t kill you makes you stronger.

The next dive was the Avaavaroa drop off. My god, did this blow my mind. An extensive coral reef that just drops off into the abyss.

Schools of fish, an eagle ray, and a couple of grey reef sharks cruised beneath us in front of a dark blue background that looked like it could engulf me at any moment. In a way, it was humbling to be on the edge of the vast, blue ocean like that.

The rest of our dives were on the northern and north-western sides of the island. Here, every time I slipped under the water, it felt like I was submerged in a woodland fairytopia.

The landscape was stunning. Here and there were crown of thorns starfish, a giant, impressive echinoderm with thorn-like ossicles containing venom. There appeared to be a healthy population here. Still, at another island within the Cook Islands called Aitutaki, their population is rampant. They are decimating the very coral they feed on.

Interestingly, on these northern dives was the amount of trash that seemed to be pulled along the floor by currents and would accumulate in hotspots around the reef and in caves. I grabbed all I could, but part of me wished to do a few dives whose sole purpose was to find as much trash as possible.

All in all, my trip to Rarotonga was fascinating. All I wanted to do once I got there was spend as much time as possible underwater, and that’s what I did. Rarotonga is a magical place, and it is so worthy of preservation. I hope to return back one day soon, maybe even to do my own research. But, for now, I’ll just keep harassing everyone’s insta feeds with Raro throwbacks.


References

1. Heukelem, W. V. (1973). Growth and life‐span of Octopus cyanea (Mollusca: Cephalopoda). Journal of Zoology169(3), 299–315.

2. Mather, J. A., & Mather, D. L. (2004). Apparent movement in a visual display: the ‘passing cloud’of Octopus cyanea (Mollusca: Cephalopoda). Journal of Zoology263(1), 89–94.

3. Sudekum, A. E., Parrish, J. D., Radtke, R. L., & Ralston, S. (1991). Life history and ecology of large jacks in undisturbed, shallow, oceanic communities. Fishery Bulletin, 89(3), 493–513.

4. Seminoff, J. A. (2004). Chelonia mydas. The IUCN Red List of Threatened Species 2004: e.T4615A11037468. http://dx.doi.org/10.2305/IUCN.UK.2004.RLTS.T4615A11037468.en

5. Mortimer, J. A. & Donnelly, M. (2008). Eretmochelys imbricata. The IUCN Red List of Threatened Species 2008: e.T8005A12881238. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T8005A12881238.en

The three carbon pumps of the ocean: biological, carbonate, and physical

Introduction

Carbon is the most critical component of all biological compounds and is exchanged around the Earth through a biogeochemical cycle (Archer, 2010). Although carbon is part of natural planetary systems, current concentrations of carbon dioxide (CO2) are the highest they have been in 14 million years, and this increase is attributed to anthropogenic activity, specifically from the Industrial Revolution of the 1700s (Etheridge et al., 1996; Falkowski et al., 2000; Zhang, Pagani, Liu, Bohaty, & DeConto, 2013). The oceanic carbon cycle is comprised of processes that cycle carbon around different areas of the ocean, the seafloor, the Earth’s interior, and the atmosphere. In pre-Industrial Revolution times, the ocean provided a net source of CO2 to the atmosphere, whereas now most of the carbon that enters the ocean comes from anthropogenic, atmospheric CO2 (Raven et al., 2005). According to Falkowski et al. (2000), the ocean is a reservoir for ~38,400 gigatons (Gt) of carbon, a vast amount when compared to the terrestrial biosphere (~2,000 Gt) and the atmosphere (~720 Gt). CO2 is diffused into the ocean’s surface waters and dissolves, now ready to enter the oceanic carbon cycle through three pumps: the biological pump, the carbonate pump, or the physical pump (Duan & Sun, 2003). The biological pump utilises autotrophy, such as photosynthesis by phytoplankton, to export carbon from the upper, sunlit ocean to the ocean interior or seafloor sediments and respire organic carbon into inorganic carbon (Emerson & Hedges, 2008). The carbonate pump is a process of ocean carbon sequestration driven by calcifying plankton, which releases CO2 back into the atmosphere but sequesters it by sinking to the seafloor (Smooth & Key, 1975); this is why this process is also referred to as the carbonate counter pump. The physical pump is the physio-chemical process whereby carbon is transported from the ocean surface to its interior, where it can be stored for hundreds of years (Ito & Follows, 2003; Toggweiler, Murnane, Carson, Gnanadesikan, & Sarmiento, 2003).

The Biological Pump

The biological pump is a process of oceanic carbon sequestration that is driven mainly by autotrophic phytoplankton that inhabits the surface waters. This method of autotrophy, photosynthesis, converts CO2 (dissolved inorganic carbon (DIC)) into organic biomass (particulate organic carbon (POC)) (Passow & Carlson, 2012; Sigman & Hain, 2012). Photosynthesis is the initial method of bringing carbon into the biological pump. It is further moved throughout the ocean by entering the food web after phytoplankton, which are primary producers at the lowest trophic level, are eaten by consumers. Carbon can then stay in the food web as higher trophic levels continuously consume organisms, or it can be released from the food web in the form of defecation or dead tissue (Passow & Carlson, 2012). This carbon sequestration process by primary production accounts for a vast majority of carbon fixation on Earth (Christina & Passow, 2007; De La Rocha, 2003).

Carbon is also moved into deep ocean currents or seafloor sediments by sinking organic matter. Organic material is formed by phytoplankton in the euphotic zone located at the surface level of the ocean. When plankton or other marine organisms eat, defecate, die, and decompose, this material, known as marine snow, begins to sink downwards (Passow & Carlson, 2012). One phytoplankton cell sinks at a rate of approximately 1 metre per day, meaning that, with an average depth of 4,000m, it can take over ten years for one carbon-carrying phytoplankton to reach the seafloor. Organic and inorganic matter, as well as expulsion of faecal matter from larger predators, aggregate to form marine snow that has a greater sinking velocity and can complete its journey to the seafloor in days (Heinze et al., 2015; Turner, 2015). Once this sinking organic biomass reaches deep-sea levels, it can enter the food web by becoming metabolic fuel for organisms that live there, including benthic organisms and deep-sea fish (Turner, 2015). Sinking matter transports an estimated 5–20 Gt of carbon to the deep ocean annually, where between 200 million–500 million tonnes of carbon is sequestered for thousands of years in seafloor sediment (Giering et al., 2020; Guidi et al., 2015; Henson et al., 2011). Any global warming-induced change on the integrity or function of phytoplanktonic populations will alter the efficiency at which POC is transported to ocean depths, with feedbacks on the rate of climate change.

With less than 0.5 Gt of sinking carbon reaching sequestration in seafloor sediment, between 44.5 Gt – 54.5 Gt of carbon is remineralised in the euphotic zone (Ducklow, Steinberg, & Buesseler, 2001) and between 5 Gt – 6 Gt of carbon is remineralised in midwater processes during particle sinking (Feely, Sabine, Schlitzer et al., 2004). Remineralisation occurs in the biological pump when heterotrophic organisms utilise organic matter produced by autotrophic organisms. They recycle the compounds from the organic form back to the inorganic form through respiration, making them available for reuse in primary production (Guidi et al., 2015). Remineralisation usually occurs with dissolved organic carbon (DOC) rather than POC because particles must typically be smaller than the organism taking it up for remineralisation (Lefevre, Denis, Lambert, & Miquel, 1996; Schulze & Mooney, 2012).

The particles that make it to the seafloor sediment may remain there for millions of years, trapping the carbon with them. Together, the processes that make up the biological pump ultimately remove carbon in its organic form from the ocean’s surface and return it to DIC in the deeper ocean. The thermohaline circulation (THC) returns deep-ocean DIC to the atmosphere on timescales that exceed millennia (the topic of THC will be explained further in “The Physical Pump”).

The Carbonate Pump

The carbonate pump is an extension of the biological pump but instead sequesters particulate inorganic carbon (PIC) and is driven by calcifying organisms (organisms that produce calcium carbonate (CaCO3) shells). The leading contributor to the carbonate pump is the calcifying plankton known as coccolithophores due to the vast quantity of their global population. Coccolithophores are eukaryotic, unicellular phytoplankton that produces overlapping calcite platelets called coccoliths and are currently one of the most significant contributors to carbonate sediments in the deep sea (Hofmann et al., 2010; Renaud, Ziveri, & Broerse, 2002). Coccolithophore production of coccoliths through the uptake of dissolved inorganic carbon and calcium produces CaCO3 and CO2, hence the alternate name of carbonate counter pump.

Ca2+ + 2HCO3- → CaCO3 + CO2 + H2O

However, some of the CO2 released in calcification can be used in photosynthesis (Mackinder, Wheeler, Schroeder, Riebesell, & Brownlee, 2012), and over extended periods coccolithophores contribute to decreased levels of atmospheric CO2. It is currently unknown as to the function of the coccolith. However, many theories have been proposed, including protection from predators or grazing zooplankton (Young, Andruleit, & Probert, 2009) or ballasting the cell for vertical migration into deeper water (Raven & Waite, 2004). The latter would be of considerable advantage to the carbonate pump in getting the carbon trapped in coccoliths to the seafloor. The most abundant species of coccolithophore is Emiliania huxleyi. It is likely to be the greatest global producer of calcite, meaning this species is an essential organism in transporting carbon from the ocean to be buried in marine sediment; they play a crucial role in the global biochemical carbon cycle (Balch, Holligan, & Kilpatrick, 1992).

The production of CaCO3 shells in calcifying organisms such as molluscs, foraminifera, coccolithophores, crustaceans, echinoderms, and corals (Zondervan, Zeebe, Rost, & Riebesell, 2001) is the central part of the carbonate pump. When CO2 dissolves in the surface layer of the ocean, it combines with water molecules. It enters into a series of chemical reactions that result in ions that calcifying organisms combine with calcium ions (Ca2+) to form CaCO3 (Zeebe & Wolf-Gladrow, 2001). Even though one CO2 molecule is released in calcification, one carbon atom becomes trapped within the CaCO3 molecule used in calcification and becomes part of the sediment once it sinks to the bottom of the ocean. This means calcification takes two carbon atoms from the environment and only releases one back into it, even though the formation of calcium carbonate shells is a source of CO2 (Mackie, McGraw, & Hunter, 2011) over the long-term calcifying organisms provide a sink for CO2.

Calcifying organisms provide a large mechanism for the downward transport of CaCO3 (Smith & Key, 1975). Dead organisms sink to the seafloor and dissolve on the way down and release carbon into deep-sea currents or reach the seafloor and build up to form CaCO3 sediments stored for large timescales. The scale at which CaCO3 makes its way down varies from species to species. For example, calcifying zooplankton (pteropods, ostracods and foraminifera) promote fast particulate inorganic carbon sequestration to the deep ocean due to the relatively large mass of their shells, which makes them sink rapidly. In comparison, calcifying phytoplankton such as coccolithophores will hardly sink individually, and even still, they have a broad range in sinking rates when they assimilate into biological aggregates. The burial of CaCO3 in deep-ocean sediment is one of the primary mechanisms to reduce atmospheric CO2 on geological timescales related to silicate weathering processes (Cartapanis, Galbraith, Bianchi, & Jaccard, 2018). Eventually, tectonic processes, including heat and pressure, transform seafloor sediments containing CaCO3 into limestone; this process locks carbon away for millions of years (Folk, 1980). Over time, these sediment layers eventually return carbon to the oceans by weathering and erosion (Gibb, 1978).

The Physical Pump

The physical pump uses different processes to transport DIC from the ocean surface to its interior. Firstly, the solubility of CO2 in water is the initial process of getting carbon into the ocean as DIC (Duan & Sun, 2003). Carbon dioxide dissolves in oceanic water and, unlike many other gases, it reacts with water to form a collective of ionic and non-ionic species (DIC), which include dissolved free carbon dioxide (CO2 (aq)), carbonic acid (H2CO3), bicarbonate (HCO3−), and CO32− (Weiss, 1974). There is a strong inverse function of seawater temperature on the solubility of CO2, as solubility is greater in colder water (Toggweiler et al., 2003). As sea surface temperature (SST) increases, less CO2 can be taken up by the ocean; the progressive warming of the oceans releases CO2 in the atmosphere because of its lower solubility in warmer seawater.

The THC is part of a global, oceanic conveyor belt, driven by heat and freshwater fluxes, where thermo refers to temperature, and haline refers to salinity, which together determines seawater’s density (Rahmstorf, 2003). The model of THC was first described by Stommel and Arons (1959), where they explored how temperature and salinity moved ocean water around the globe. Seawater with higher temperatures expands and is less dense than seawater at lower temperatures (Millero, Gonzalez, & Ward, 1976). Seawater with higher salinity is denser than seawater with lower salt content (Millero et al., 1976). Seawater with lower density floats over denser seawater; this is known as stable stratification (Maiti, Gupta, & Bhattacharyya, 2008). When dense seawater masses are initially formed, they are not stably stratified and will seek to correctly locate themselves vertically by their density and become stably stratified. This stratification process is the main driving force behind deep ocean currents, which carry carbon that has sunk from surface layers on the global conveyor belt, essentially sequestering it for hundreds of years.

The process of denser seawater joining the global conveyor belt is called downwelling. Higher density water accumulates and sinks below lower density water at places within the ocean where warm rings spin clockwise and create surface convergence, pushing the surface water downwards (Rao, Joshi, & Ravichandran, 2008; Yang, 2009). These areas of downwelling bring large amounts of carbon from the surface waters to be sequestered down below. Alternately, upwelling brings dense, cooler water to the surface to replace the warmer surface water. This water is usually nutrient-rich, including dissolved CO2, meaning that these areas of upwelling provide an ideal location for an abundance of phytoplankton to carry out primary production and ultimately recycle the carbon brought to the surface from the deep ocean (Sarhan, Lafuente, Vargas, Vargas, & Plaza, 2000)

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The effect of ocean acidification on calcareous phytoplankton due to human-induced climate change

Introduction

Humans have begun to drastically alter the atmospheric environment since the Industrial Revolution of the 1700s, where the burning of fossil fuels released exponential amounts of carbon dioxide into the air. Along with increasing the global temperature, affecting life cycles of organisms, and disassembling natural species interactions, this release initiated a process known as ocean acidification, whereby the pH of the ocean has decreased from 8.2 to 8.1 (Feely, Doney, & Cooley, 2009). The effect that ocean acidification has on marine organisms starts at the base of the food chain with primary producers, such as phytoplankton, and repercussions can then be seen throughout entire food webs. Calcareous phytoplankton (i.e., coccolithophores) may be at high risk of impact from ocean acidification due to the calcium carbonate plates that they produce through calcification. Coccolithophores are key players in the global biogeochemical cycle, the pelagic food chain, and oxygen production through photosynthesis, so any negative impacts that ocean acidification may have on them need to be understood and mitigated for the health and wellbeing of humankind.

Climate change

Climate change refers to global climatic shifts that were intensified in the mid-20th century through the burning of fossil fuels (Griffin, 2018). This anthropogenic influence has resulted in an increasing amount of carbon dioxide (CO2) in the atmosphere with a >90% probability that the observed average global temperature increase is due to human-induced greenhouse gas concentrations and around half of this increase occurring in the last three decades (Feely et al., 2009; Rosenzweig et al., 2008). Anderson, Hawkins, and Jones (2016) describe the greenhouse effect as infrared energy that has been re-emitted from solar radiation is absorbed by water vapour and CO2 to create a ‘blanket’ around planet Earth. As CO2 concentrations increase, this greenhouse effect is enhanced, and the planet warms further beyond its natural average temperature.

Regional warming exhibits observable biological changes in terrestrial systems. Included amongst these changes are increases in coastal erosion (Beaulieu & Allard, 2003; Forbes, Parkes, Manson, & Ketch; 2004; Orviku, Jaagus, Kont, Ratas, & Rivis, 2003), melting permafrost (Frauenfeld, Zhang, Barry, & Gilichinsky, 2004), and glaciers shrinking in all seven continents (Oerlemans, 2005). Natural increases and decreases in Earth’s temperature have been recorded over millions of years (Savin, 1977), which can add scepticism to the idea that current global heating is due to anthropogenic activity rather than part of a natural cycle. A study by Reichert, Bengtsson, and Oerlemans (2002) into Swiss and Norwegian glacial retreat showed that the retreat could not be due to natural climatic change because it exceeds glacial fluctuations derived from the general circulation model, meaning that another force must be acting on the glaciers.

Climate change’s effects also reach the ocean. Edwards and Richardson (2004) describe phenological changes that occur in the wake of a warming ocean. An increase in sea surface temperature (SST) is used as an indicator for climate change, and it affected the seasonal development and phenology of plankton species. Massive phenological changes occurred at a 0.9oC increase of SST. The extent of these changes was more significant than those of terrestrial studies (Root et al., 2003), which may indicate that marine communities have heightened sensitivity to climate change. Furthermore, Edwards and Richardson’s (2004) study showed there was a different rate of response in communities to ocean warming, creating a “mismatch between successive trophic levels and a change in the synchrony of timing between primary, secondary and tertiary production” (p. 883). This mismatch will directly affect populations at higher trophic levels, including commercial fish species, marine mammals, and seabirds, and adaption will need to take place to realign these trophic levels with primary production. Not only are higher trophic levels at risk in response to changing phenology of plankton due to climate change, but other essential ecosystem services will be impacted, including the production of oxygen that we breathe, the sequestration of CO2, and the biogeochemical cycling of nitrogen, phosphorus, and silica (Richardson & Schoeman, 2004). Beaugrand and Reid (2003) study provided evidence for climate change-induced, long-term changes to the three trophic levels of phytoplankton, zooplankton, and salmon. Various declines and increases of phytoplankton and zooplankton ensued due to regional temperature increases over time, which caused the ultimate decline of salmon stocks in 1988, and this decline is expected to continue as the climate proceeds to change.

Ocean acidification

The ocean has absorbed approximately one-quarter of anthropogenically emitted CO2 over the industrial era, causing chemical reactions that reduce oceanic pH, concentrations of carbonate ions (CO32-), and saturation states of two calcium carbonate (CaCO3) minerals calcite and aragonite; this is the process of ocean acidification (OA) (Feely et al., 2009). The ocean absorbs CO2 in two ways: through photosynthesis undertaken by marine phytoplankton (Rost, Riebesell, & Burkhardt, 2003) and through the dissolving of CO2 in seawater (Feely et al., 2009). When CO2 reacts with seawater, it creates carbonic acid (H2CO3), which dissociates to hydrogen ions (H+) that combine with carbonate to form bicarbonate ions (HCO3-). As atmospheric CO2 increases, the ocean continually absorbs greater amounts of CO2, and as temperature increases, CO2 leaks out of the ocean back into the atmosphere. As CO2 is absorbed, carbonate gets used up and must be replaced by stocks from the deeper ocean. Currents bring water with fresh carbonate to the surface and circulate water carrying the captured carbon into the ocean. As SST increases, this circulation process becomes more difficult, and the ocean stratifies. The surface water begins to saturate with CO2, decreasing support for phytoplankton, and photosynthetic CO2 uptake slows. Feely et al. (2009) reported the average pH of the ocean since the industrial era to have decreased by 0.11 pH units (29% acid concentration increase) and predicted a further decrease of 0.3 pH units (150% acid concentration increase) by 2100.

Marine organisms (e.g. coral, bivalves) extract bicarbonate ions from seawater to form skeletons or shells in a process called calcification:

Ca2+ + 2HCO3- → CaCO3 + CO2 + H2O

Calcification is a source of CO2 and is balanced by weathering, a process where rainwater reacts with carbonate rocks and consumes atmospheric CO2 on its way to rivers:

CaCO3 + CO2 + H2O → Ca2+ + 2HCO3-

A decline in the availability of carbonate ions will affect the degree of carbonate polymorph saturation in seawater, therefore compromising marine organisms’ ability to construct their skeletons/shells (Gledhill, Wanninkhof, & Eakin, 2009). A study by Gattuso et al. (2009) examined OA’s ability to affect the calcification of calcareous plankton, realising that any changes experienced by calcified taxa may alter the oceans’ ability to act as a global carbon sink. Calcareous, planktonic foraminifera observations from the Southern Ocean showed a decrease in shell weight compared to older records, with the implication that OA is the causing factor (Moy, Howard, Bray, & Trull, 2009). Suppose OA can change the morphology of a species and consequently affect multiple species up the trophic levels. In that case, the question is whether these species will cope with the effects of acidification through adaptation. This was highlighted in an experiment by Bibby, Cleall-Harding, Rundle, Widdicombe, and Spicer (2007) who observed the effects of acidification on the defence mechanisms of the periwinkle Littorina littorea toward its predator the green shore crab Carcinus meanus. L. littorea can reinforce their calcified shells when experiencing extensive predation pressure, with snails exposed to C. meanus for 15 days producing shells that were 30% thicker than those that were not under predation pressure. At reduced seawater pH, L. littorea could not thicken their shell and compensated by altering their behaviour to avoid the crabs. This shows that adaptation is possible, but at what cost? Behavioural alteration in L. littorea could mean they spend less time feeding, or it could affect their interactions with other species with unknown consequences.

Coccolithophores

Diversity of coccolithophores. (A) Coccolithus pelagicus, (B) Calcidiscus leptoporus, (C) Braarudosphaera bigelowii, (D) Gephyrocapsa oceanica, (E) E. huxleyi, (F) Discosphaera tubifera, (G) Rhabdosphaera clavigera, (H) Calciosolenia murrayi, (I) Umbellosphaera irregularis, (J) Gladiolithus flabellatus, (K and L) Florisphaera profunda, (M) Syracosphaera pulchra, and (N) Helicosphaera carteri.
By Monteiro, F.M., Bach, L.T., Brownlee, C., Bown, P., Rickaby, R.E., Poulton, A.J., Tyrrell, T., Beaufort, L., Dutkiewicz, S., Gibbs, S. and Gutowska, M.A. – https://advances.sciencemag.org/content/2/7/e1501822, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=91145677
Umbilicosphaera sibogae coccolithophore conglomeration taken with ZEISS MERLIN Scanning Electron Microscope. By ZEISS Microscopy – CC BY-NC-ND 2.0, https://www.flickr.com/photos/zeissmicro/6908938729

Coccolithophores are unicellular, eukaryotic, calcareous phytoplankton that produces overlapping calcite platelets called coccoliths and are presently one of the main primary producers of the open ocean and significant contributors to carbonate sediments in the deep sea. (Hofmann et al., 2010; Renaud, Ziveri, & Broerse, 2002). Coccolithophores produce coccoliths through the uptake of dissolved inorganic carbon and calcium, and CaCO3 and CO2 are produced. Some of the CO2 released in calcification can be used in photosynthesis (Mackinder, Wheeler, Schroeder, Riebesell, & Brownlee, 2012). It is possible that over long periods, coccolithophores may contribute to decreased levels of atmospheric CO2. Even though one CO2 molecule is released in calcification, one carbon atom becomes trapped within the CaCO3 molecule used to make coccoliths and becomes part of the sediment once it sinks to the bottom of the ocean. This means calcification takes two carbon atoms from the environment and only releases one back into it. Even though the formation of calcium carbonate shells is a source of CO2, over the long-term coccolithophores provide a sink for CO2 (Mackie, McGraw, & Hunter, 2011). It is currently unknown as to the function of the coccolith, but many theories have been proposed. These include protection from predators or grazing zooplankton (Young, Andruleit, & Probert, 2009), ballasting the cell for vertical migration into deeper, more nutrient-rich water (Raven & Waite, 2004), protection from virus infection (Raven & Waite, 2004), or aiding in the filtering of non-photosynthetically active radiation at the surface to aid in photosynthesis or focussing light to the chloroplasts in deeper water (Raven & Crawfurd, 2012).

The most abundant species of coccolithophore is Emiliania huxleyi. It is likely to be the greatest global producer of calcite, meaning this species is an essential organism in transporting carbon from the ocean to be buried in marine sediment; they play a crucial role in the global biochemical carbon cycle (Balch, Holligan, & Kilpatrick, 1992). As the most abundant species, this also means that E. huxleyi is a key organism in the marine pelagic system, where the base of the food web is comprised of over 5,000 species of phytoplankton (Rost & Riebesell, 2004). Among this vast array of species, only a few select taxonomic groups are responsible for most of the pelagic systems primary production, one of these is coccolithophores and therefore reinforces their importance in the oceanic ecosystem. Coccolithophores are sensitive to nitrogen, phosphorus, and silicate ratios in the water, inducing competitive dominance between coccolithophores and other phytoplanktonic communities such as diatoms, microflagellates, and dinoflagellates. Anthropogenic interference with these ratios comes in the form of agricultural runoff leading to eutrophication and increasing nitrogen in seawater, causing coccolithophores to form blooms in these favourable environments and outcompete other species (Yunev et al., 2007). As agriculture and the use of nitrogen-based pesticides increases, more runoff makes its way to the ocean, which could see a tip in the balance of conditions to favour coccolithophore species of phytoplankton. From there, will other phytoplankton species be able to adapt in time, or will they be outcompeted and eventually become extinct?

As OA decreases carbonate saturation in seawater, coccolithophores ability to produce coccoliths may be inhibited as the increase in atmospheric CO2 may affect their calcification mechanisms. When environments change, some organisms adapt to suit their changing environment, so as ocean pH decreases, will coccolithophores have an evolutionary response? Beaufort et al. (2011) found that coccolithophores have channels to pump out H+ ions during calcification to avoid acidosis. Furthermore, a feedback loop is created because when the function of these channels is disrupted, calcification is halted. This study provided evidence that increased oceanic CO2 concentrations decreased coccolith mass as OA impairs the normal function of ion channels and places selection pressure on coccolithophore’s calcification rates (Tyrell, Holligan, & Mobley, 1999). Flynn, Clark, and Wheeler (2016) found that coccolithophores put under OA conditions showed selection for lower calcification rates to avoid the risk of acidosis at higher H+ concentrations. They predicted coccolithophore calcification would decrease by 25% as OA continued and atmospheric CO2 reached 750 ppm (an increase of 335.62 ppm from current atmospheric CO2 levels). Conversely, a long-term study of an E. huxleyi population that was allowed to reproduce for 700 generations under conditions similar to those predicted for the year 2100 showed their population could adapt and increase calcification and CaCO3 content (Benner et al., 2013). This contrasts with other short-term experiments and shows that long-term OA exposure could alter calcification responses in E. huxleyi, and potentially other calcareous phytoplankton as well. Similarly to this experiment, Smith et al. (2012) found naturally forming populations of highly calcified coccolithophores in water with low CaCO3 saturations.

The Paleocene-Eocene Thermal Maximum (PETM) occurred approximately 55.5 million years ago and saw a global temperature increase of 5–8 °C and ~12,000 gigatons of carbon released over 50,000 years (0.24 gigaton per year) (McInherney & Wing, 2011). Today, the anthropogenic release of carbon is equal to 10 gigatons of carbon per year; therefore, it will only take 1,200 years for 12,000 gigatons of carbon to be released as in the PETM. It has been shown that there was no change in coccolithophore distribution attributed to acidification in the PETM (Beaufort et al., 2011; Iglesias-Rodriguez et al., 2008), meaning that they were likely able to adapt over the 50,000 years of exposure to increasing carbon levels. Will 1,200 years be enough time for them to adapt again? Results from studies about the effect OA has on coccolithophores contradict one another. Different experiment environments show different outcomes, including short-term experiments vs long-term experiments, different coccolithophore species, and different regional populations of coccolithophores (Beaufort et al., 2011; Benner et al. 2013; Flynn et al., 2016; Smith et al., 2012). An alternative way to look at the discrepancies seen between experiments is that studies about the effects of OA are often hypothesised to have a negative outcome. If it is looked at that a decreased pH is a more favourable condition to coccolithophores, rather than the alternative, it can explain why highly calcified coccolithophores can be found in conditions of low CaCO3. In this scenario, they would have bioengineered their higher pH environment to a more favourable, lower one through calcification and the release of CO2, creating highly calcified individuals. Once they “created” an environment with favourable pH that now had low concentrations of CaCO3, they would no longer need the CaCO3. In some studies, at low pH environments, coccolith growth appeared to be inhibited. However, perhaps the coccolithophores were satisfied with the pH in their environment and therefore did not need to alter it further through calcification. But, I digress. What are your thoughts on the matter?

Conclusion

Anthropogenically induced climate change has a clear impact on natural, global processes, specifically the ocean’s role in balancing CO2 levels in the atmosphere. Coccolithophores play a part in this role by producing vast amounts of calcite and acting as a carbon sink. The effects of ocean acidification on coccolithophores have been explored through previous studies and experimentation, with multiple conclusions drawn. This makes it difficult to understand how catastrophic the effects of ocean acidification will be in the future as atmospheric CO2 continues to rise, primarily because any changes to coccolithophores will have direct and indirect consequences for other taxa and ecosystem processes. Alternatively, coccolithophores might be environmental bioengineers and use calcification to alter oceanic pH levels to suit their environment. Further research is essential to narrow down coccolithophores precise role in the ecosystem, determine the reason for their coccoliths, discover if they can adapt to a changing environment and how quickly they can do this, and establish the effect ocean acidification has had on them and can potentially have on them in the future, and what will this mean for the world.


References

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Bates, N. R., Michaels, A. F., & Knap, A. H. (1996). Alkalinity changes in the Sargasso Sea: geochemical evidence of calcification?. Marine Chemistry, 51(4), 347–358.

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Beaulieu, N., & Allard, M. (2003). The impact of climate change on an emerging coastline affected by discontinuous permafrost: Manitounuk Strait, northern Quebec. Canadian Journal of Earth Sciences, 40(10), 1393–1404.

Benner, I., Diner, R. E., Lefebvre, S. C., Li, D., Komada, T., Carpenter, E. J., & Stillman, J. H. (2013). Emiliania huxleyi increases calcification but not expression of calcification-related genes in long-term exposure to elevated temperature and p CO2. Philosophical Transactions of the Royal Society B: Biological Sciences, 368(1627), 20130049.

Bibby, R., Cleall-Harding, P., Rundle, S., Widdicombe, S., & Spicer, J. (2007). Ocean acidification disrupts induced defences in the intertidal gastropod Littorina littorea. Biology letters, 3(6), 699–701.

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Iglesias-Rodriguez, M. D., Halloran, P. R., Rickaby, R. E., Hall, I. R., Colmenero-Hidalgo, E., Gittins, J. R., … & Boessenkool, K. P. (2008). Phytoplankton calcification in a high-CO2 world. science, 320(5874), 336–340.

Mackie, D., McGraw, C., & Hunter, H. (2011). OA not Ok: An introduction to the chemistry of Ocean Acidification. The University of Otago, 4–41.

Mackinder, L., Wheeler, G., Schroeder, D., Riebesell, U., & Brownlee, C. (2010). Molecular mechanisms underlying calcification in coccolithophores. Geomicrobiology, 27(6–7), 585–595. doi: 10.1080/01490451003703014

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Renaud, S., Ziveri, P., & Broerse, A. T. (2002). Geographical and seasonal differences in morphology and dynamics of the coccolithophore Calcidiscus leptoporus. Marine Micropaleontology, 46(3-4), 363–385.

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Smith, H. E., Tyrrell, T., Charalampopoulou, A., Dumousseaud, C., Legge, O. J., Birchenough, S., … & Hydes, D. J. (2012). Predominance of heavily calcified coccolithophores at low CaCO3 saturation during winter in the Bay of Biscay. Proceedings of the National Academy of Sciences, 109(23), 8845–8849.

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Phylum Echinodermata: sea stars, sand dollars, urchins, and cucumbers

Introduction

Echinoderms are the largest marine-only phylum, and its ~7,000 species are found at every ocean depth from rock pools to the deep abyss (Dubois, 2014). Sea stars, sea urchins, sand dollars, and sea cucumbers comprise this phylum and let me tell you why they’re so darn cool.

Morphology

Echinoderms all possess radial symmetry, even though this can be quite hard to see in sea cucumbers, trust me, it’s there. Usually, the oral surface is on the underside of the animal, and the anus is located on top. The calcareous echinoderm endoskeleton is composed of ossicles which can be in the form of plates, spines, or lumps (Evamy & Shearman, 1965). The ossicles form a sponge-like structure called the stereom and are supported by a tough epidermis (Bottjer, Davidson, Peterson, & Cameron, 2006). Each ossicle develops from the deposition of a single cell which divides into more cells that deposit calcium carbonate in the original orientation. Ossicles are connected by collagen and may connect to muscles, allowing for flexibility and manoeuvrability. Spines are modified ossicles used for protection, locomotion, burrowing, gathering food and can also contain venom.

Pedicellaria

Pedicellariae are small, pincer-like structures used for protection against anything that may settle or graze on an animal’s body (Campbell, 2020; Coppard, Kroh, & Smith, 2012). Some pedicellariae are involved in capturing food, and some may be venomous. Each pedicellaria has its own muscles and sensory receptors, and therefore each pedicellaria is capable of reacting to a stimulus. There are four types of pedicellaria in urchins and two types for sea stars; one animal may have multiple types.

Pedicellaria of a crown-of-thorns sea star (Acanthaster planci).
By Philippe Bourjon – The uploader on Wikimedia Commons received this from the author/copyright holder., CC BY 3.0, https://commons.wikimedia.org/w/index.php?curid=18009032.
The incredibly dangerous flower urchin (Toxopneustes pileolus) with its long, venomous pedicellariae.
By Vincent C. Chen – Own work, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=11721803.

Water-vascular system

Before we dive into this topic, take a look at this diagram, and feel free to refer to it as we dive into the incredibly unique water-vascular system.

Basic anatomy of an echinoderm. By CNX OpenStax, CC BY 4.0, https://commons.wikimedia.org/wiki/File:Figure_28_05_01.jpg.

The water vascular system is an elaborate closed system of canals used to help locomote the organism via its tube feet (Blake & Guensburg, 1988; Prusch & Whoriskey, 1976). The madreporite is a small sieve filter that creates an external link to the water-vascular system and is usually located to one side of the aboral surface and connects to a stone canal that extends vertically until it meets the ring canal. Radial canals emerge from the ring canal to the rays of the body in sea stars and around the body in sea urchins. From the radial canal stem lateral canals, which connect to ampullae and tube feet. Ampullae are bulb-like swellings that serve as reservoirs for water and fill the tube foot with water as they contract.

Tube feet have suction cup endings allowing for strong attachment to substrata and provide a general direction of movement. Pressure is exerted on the end of the sucker, and mucous functions as an adhesive. When the tissue inside the sucker contracts, it forms a cup that is secured to the substrate. In the case of sea stars living on soft substrates, tube feet are pointy so they can penetrate sediment and bury themselves.

Tube feet of the helmet urchin (Colobocentrotus atratus).
By Sébastien Vasquez – The uploader on Wikimedia Commons received this from the author/copyright holder., CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=40284469.

Feeding

The feeding strategies differ significantly between species of Echinodermata. Some are filter feeders, most urchins are grazers, and most sea stars are carnivorous predators.

This predatory strategy of sea stars is perhaps the most interesting of the echinoderms (Melarange, Potton, Thorndyke, & Elphick, 1999; Semmens et al., 2013; Wulff, 1995). The oesophagus connects to a stomach with two sections called the cardiac stomach and the pyloric stomach. In evolutionarily advanced sea stars, the cardiac stomach can be everted out of the mouth and engulf and digest food. They can use their tube feet to create suction on bivalve shells and open them, where they will evert a section of their cardiac stomach inside the shell to release enzymes to digest the animal inside. The stomach retracts back inside and the partially digested prey can be passed to the pyloric stomach.

A starfish (Circeaster pullus) everting its cardiac stomach to feed on coral.
By NOAA – Flickr, CC BY-SA 2.0, https://commons.wikimedia.org/w/index.php?curid=47949152.

Regular vs Irregular Echinoids

Regular echinoids (e.g., sea urchin) have no front or back end, and the oral end is underneath and the aboral end is on top. From above, they are circular and radially symmetrical because regular echinoids roam the seafloor in search of food and need to move in any direction. This means they are exposed to predators and have evolved elaborate spines for defence and locomotion. Spines vary between species: needle-like, club-like, poisonous, or thorny. Regular echinoids are usually scavengers with a diet of plant matter, animal detritus, and other inverts, and can use their tube feet to grasp food. They have powerful, complex jaws called Aristotle’s Lanterns, which extend through the mouth to collect food and leave a distinctive star-shaped grazing trace.

Irregular echinoids (e.g., sand dollars) lead different lifestyles from the regulars. They burrow in the seafloor and extract nutrients from sediment and have one plane of symmetry – the oral end is at the front of the animal to collect food, and the aboral end is at the rear to leave waste behind. The spines have lost their defensive role and have become reduced and hair-like to help burrow, move through sediment, gather food, and generate currents in the burrow. Many have lost their jaws as they are unnecessary to their mode of life. The tube feet are modified into flanges for respiration and gathering food.

Classifications

Class Echinoidea

Class Echinoidea, aka echinoids, is composed of sea urchins and sand dollars.

Top – West Indian sea egg (Tripneustes ventricosus). Bottom – reef urchin (Echinometra viridis).
By Nhobgood, Nick Hobgood – Own work, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=11449176.
Lateral view of Aristotle’s Lantern of a sea urchin.
By Philippe Bourjon – The uploader on Wikimedia Commons received this from the author/copyright holder, CC BY-SA 4.0, https://commons.wikimedia.org/w/index.php?curid=35659671.
Sand dollar (Mellita species) burying itself in the sand.
By John Tracy from Snellville, GA, USA – End of the line, CC BY 2.0, https://commons.wikimedia.org/w/index.php?curid=26620303.

Class Holothuroidea

Sea cucumbers have leathery skin and an elongated body that is radially symmetrical along its longitudinal axis. They have no oral or aboral surface but instead, stand on one of their sides. Extraordinarily, they can loosen or tighten the collagen that forms their body wall and can essentially liquefy their body to squeeze through small gaps.

Brown sea cucumber (Actinopyga echinites) displaying its feeding tentacles and tube feet.
By François Michonneau – d2008-Kosrae-0084.jpg, CC BY 3.0, https://commons.wikimedia.org/w/index.php?curid=20189778.
A giant sea cucumber (Thelenota ananas).
By Leonard Low from Australia – Flickr, CC BY 2.0, https://commons.wikimedia.org/w/index.php?curid=1552175.

Class Asteroidea

There are around 1,500 species of sea star that make up the class Asteroidea.

Necklace sea star (Fromia monilis).
By Nhobgood Nick Hobgood – Own work, CC BY-SA 3.0, https://commons.wikimedia.org/w/index.php?curid=6279893.
Crown-of-thorns sea star (Acanthaster planci) is one of the largest sea stars, and it gets its name from the venomous, thorny ossicles covering its surface.
By jon hanson on flickr. – https://www.flickr.com/photos/jonhanson/89930167/, CC BY-SA 2.0, https://commons.wikimedia.org/w/index.php?curid=665552.

References

Blake, D. B., & Guensburg, T. E. (1988). The water vascular system and functional morphology of Paleozoic asteroids. Lethaia, 21(3), 189–206.

Bottjer, D. J., Davidson, E. H., Peterson, K. J., & Cameron, R. A. (2006). Paleogenomics of echinoderms. Science, 314(5801), 956–960.

Campbell, A. C. (2020). Form and function of pedicellariae. In Echinoderm studies (pp. 139-167). CRC Press.

Coppard, S. E., Kroh, A., & Smith, A. B. (2012). The evolution of pedicellariae in echinoids: an arms race against pests and parasites. Acta Zoologica, 93(2), 125–148.

Dubois, P. (2014). The skeleton of postmetamorphic echinoderms in a changing world. The Biological Bulletin, 226(3), 223–236.

Evamy, B. D., & Shearman, D. J. (1965). The development of overgrowths from echinoderm fragments. Sedimentology, 5(3), 211–233.

Melarange, R., Potton, D. J., Thorndyke, M. C., & Elphick, M. R. (1999). SALMFamide neuropeptides cause relaxation and eversion of the cardiac stomach in starfish. Proceedings of the Royal Society of London. Series B: Biological Sciences, 266(1430), 1785–1789.

Prusch, R. D., & Whoriskey, F. (1976). Maintenance of fluid volume in the starfish water vascular system. Nature, 262(5569), 577–578.

Semmens, D. C., Dane, R. E., Pancholi, M. R., Slade, S. E., Scrivens, J. H., & Elphick, M. R. (2013). Discovery of a novel neurophysin-associated neuropeptide that triggers cardiac stomach contraction and retraction in starfish. Journal of Experimental Biology, 216(21), 4047–4053.

Wulff, L. (1995). Sponge-feeding by the Caribbean starfish Oreaster reticulatus. Marine Biology, 123(2), 313–325.

Phylum Arthropoda: the largest phylum in the animal kingdom

Introduction

Arthropoda: you may remember them from such fears as arachnophobia and your recent nightmare, “Help! I’m Locked in a Coffin of Cockroaches!” But, no fear, I won’t be burdening you with any terrestrial garbage because, as you know, it’s all underwater from here.

Morphology

To qualify for Phylum Arthropoda, you must be one of over 10 million species that lack a backbone, have an exoskeleton, segmentation, bilateral symmetry, a coelom, and paired, jointed appendages. Their segments are grouped into body divisions called tagmata, where segments and limbs have specialised functions; the three tagmata are the head, thorax, and abdomen, although some species have a combined head and thorax called a cephalothorax.

Exoskeleton

Arthropod exoskeletons are a cuticle that is secreted by the epidermis and is composed of two layers which aid in support and protection (Chen, Lin, McKittrick, & Meyers, 2008). The thin, waxy outer layer is called the epicuticle and is used in waterproofing. The thick, inner layer is called the procuticle and is the central structural part composing the majority of the exoskeleton. The exoskeleton is attached to the soft body by muscles and the animal uses those muscles to flex their joints (although some use hydraulic pressure to extend them).

Moulting

The exoskeleton is not flexible and, therefore, restricts arthropod growth. In order to grow, arthropods moult and shed the old exoskeleton in an almost continuous cycle until they reach their full size. First, the epidermis secretes a moulting enzyme that separates the old cuticle from the body. While the old cuticle is detaching, the epidermis secretes a new layer that will form part of the procuticle. After this is complete, the animal will take on seawater to split the old cuticle along predetermined weaknesses, and the animal will crawl out of its old exoskeleton. The new cuticle is exceptionally soft, and the animal is highly vulnerable as it continues to pump itself up with seawater to stretch the soft cuticle out. The cuticle will harden, and the animal can relax and eat its old exoskeleton to get back some nutrients (this gives me big Goldmember vibes iykyk).

Subphylum Crustacea

Crustaceans are what I like to call the insects of the ocean, and incudes isopods, copepods, barnacles, shrimp, krill, crabs, lobsters… the list goes on.

Appendages

The head region contains two pairs of sensory antennae, mandibles for crushing food, and first and second maxillae to sort and deliver food to the mandibles. The thoracic regions appendages are called thoracopods and may be specialised into maxillipeds which are specialised for feeding, and pereiopods, specialised for walking and swimming. The abdominal region contains pleopods which can be specialised for swimming, jumping, respiration, egg brooding, or copulation. The final pleopods may modify into a tail called a uropod. The abdomen terminates at the telson, which usually sits above the uropod and contains excretory organs. The number and diversity of appendages vary from amongst crustacean species.

File:Anatomy of a shrimp 3.jpg - Wikimedia Commons
The appendages of a shrimp: A: antennae. R: rostrum. C: carapace. Mx: maxilliped. U: uropod. T: telson. P: pereiopod. Pl: pleopod. 1–9: abdominal segments.

Crustaceans usually have biramous appendages that branch into two, where each branch consists of a series of segments attached end-to-end. The branching takes place on the second article. The external branch of the appendages is known as the exopodite, while the internal branch is known as the endopodite. Crustacean appendages have adapted to function in sensing their environment, defending against predators, swimming, walking, grasping, transferring sperm, generating water movement, and gas exchange. Some crustaceans have uniramous appendages thought to result from evolutionary loss of the second branch.

The difference between biramous and uniramous appendages within the phylum Arthropoda.

Classifications

Class Cirripedia

The most famous cirripeds are the acorn and gooseneck barnacles, and they live attached to hard substrates (Doyle, Mather, Bennett, & Bussell, 1996). They have a hard carapace made from calcareous plates that enclose the soft body parts. Their thoracic appendages are called cirri, which are biramous. The endopodites and exopodites are covered with setae to filter food particles from the water; they can also respire through the cirri. Most barnacles are hermaphroditic, and the penis extends into neighbouring barnacles to deposit spermatophores (Charnov, 2018). The larvae are planktonic and moult until they find a suitable substrate in which they settle on their “back”, the carapace, which adheres permanently to the substrate.

Gooseneck barnacles (order Pedunculata) growing in a tidal cave.
Northern acorn barnacles (Semibalanus balanoides).

Order Amphipoda and Order Isopoda

Amphipods are the most annoying crustacean. They’re the ones that bite you at the beach, aka sandflies. Isopods are similar in some ways but are lice. Let me break them both down for you.

Amphipods are scavengers and consume smaller invertebrates and plant matter; that’s why you often find them around driftwood or decaying seaweed at the beach. They are frequently consumed therefore making them an integral part of coastal food webs. Their bodies are laterally compressed (flattened from side to side) with no carapace and have the three main arthropod tagmata. They have strong uropods which aid them in jumping all over your lovely picnic.

A freshwater amphipod species (Gammarus roeseli).

Isopods have a range of feeding strategies from scavengers to carnivores and parasites to filter feeders. Their bodies are dorsoventrally flattened (flattened top to bottom, creating a wide, flat profile), and they lack a prominent carapace; it’s more of a helmet, if anything. Like amphipods, they contain all three main body parts and have a pleotelson where the last abdominal segment is fused with the telson.

A carnivorous isopod called the speckled sea louse (Eurydice pulchra).
A giant, marine isopod (Bathynomus giganteus).

Order Decapoda

Decapods, meaning “ten-footed”, are your supermarket crustaceans, e.g., crabs, lobsters, prawns, and shrimps, although I’m sure you’ll agree they look a lot better in the ocean! One of their thoracic appendages may be specialised into large pincers called chelae (think lobster claws), used to crush shells, tear up food, and pass pieces to the maxillipeds. The maxillipeds are the first three pairs of thoracic appendages and are modified for feeding. The abdominal appendages function to carry eggs, brood young, or transfer spermatophores. They usually have a uropod and telson that serve as a strong tail. Although, some decapods, e.g., crabs, have short abdomens, which are typically folded under the thorax. In males, this fold is triangular, and in females, it is broader so it can hold the eggs. Their carapace extends low enough to cover their gills.

Many decapod species can demonstrate the ability to autotomise, whereby they can regenerate an appendage after it has been dropped (Juanes & Smith, 1995; Shinji, Miyanishi, Gotoh, & Kaneko, 2016). They usually drop their limbs when threatened by a predator as a deterrent; the predator will be distracted by the limb, and the decapod can escape. A blot clot will prevent bleeding, and regeneration of the new limb will start immediately and can usually be seen after the successive moult. Growing a new appendage is extremely energy taxing, so dropping it in the first place is usually a last resort.

European lobster (Homarus gammarus).
Purple rock crab (Leptograpsus variegatus).
Mantis shrimp (Odontodactylus scyllarus).

References

Charnov, E. L. (2018). Sexuality and hermaphroditism in barnacles: a natural selection approach. In Barnacle biology (pp. 89–103). Routledge.

Chen, P. Y., Lin, A. Y. M., McKittrick, J., & Meyers, M. A. (2008). Structure and mechanical properties of crab exoskeletons. Acta biomaterialia, 4(3), 587–596.

Doyle, P., Mather, A. E., Bennett, M. R., & Bussell, M. A. (1996). Miocene barnacle assemblages from southern Spain and their palaeoenvironmental significance. Lethaia, 29(3), 267–274.

Juanes, F., & Smith, L. D. (1995). The ecological consequences of limb damage and loss in decapod crustaceans: a review and prospectus. Journal of Experimental Marine Biology and Ecology, 193(1-2), 197–223.

Shinji, J., Miyanishi, H., Gotoh, H., & Kaneko, T. (2016). Appendage regeneration after autotomy is mediated by Baboon in the crayfish Procambarus fallax f. virginalis Martin, Dorn, Kawai, Heiden and Scholtz, 2010 (Decapoda: Astacoidea: Cambaridae). Journal of Crustacean Biology, 36(5), 649–657.

Worms: Phylum Platyhelminthes, Nemertea, Nematoda, and Annelida

Introduction

Why is it that every terrestrial creepy-crawly seems to have a marine counterpart? Slaters? How about isopods. Spiders? Try crabs. Worms? Well, let me tell you. I’ve got flatworms, I’ve got ribbon worms, I’ve even got roundworms, and you can bet your ass I’ve got ringed worms.

Phylum Platyhelminthes

Flatworms are simple folk; they are acoelomates (have no body cavity) and are restricted to a flattened body shape due to a lack of circulatory and respiratory organs. They do, however, have nervous ganglia and longitudinal nerve trunks running along their bodies. They are bilaterians and have three cell layers (endoderm, mesoderm, ectoderm) and have protonephridia which functions similarly to a kidney. Flatworms can be colourful or dull.

Flatworm of the Eurylepta species.
Dawn flatworm (Pseudobiceros hancockanus).

Class Turbellaria

Turbellarians are the more traditional class of flatworms and are represented by around 4,500 species. Most species are externally ciliated, and some have a duo-gland, an adhesive system that excretes mucous and other sticky materials to repeatedly attach and release the animal to substrates (Jennings, 1957).

The most interesting thing about Turbellarians is their reproductive strategy. All are hermaphrodites, and many of them asexually reproduce, but some species engage in a delicate, lovemaking episode known as penis fencing (Chim, Ong, & Gan, 2015; Collins III, 2017). Two flatworms will rear up, exposing two penises, and attempt to inseminate one another in a battle that can last up to an hour. They are fighting because the winner will inseminate the other and essentially become the father, free of all paternal duties and can swim away and continue with his life; the one who is inseminated must now work harder to gain the extra energy required to produce offspring.

Two flatworms (Pseudobiceros bedfordi) show off their penises in the penis fencing ritual.

Phylum Nemertea

These are the ribbon worms, and they move slowly with either their external cilia to glide on a trail of slime, muscular crawling, or undulated swimming. Similarly to flatworms, they are acoelomates and have a similar reproductive system, yet they differ in that they have a complete gut, circulatory system, and a proboscis.

The proboscis is an infolding of the body wall, and hydrostatic pressure “fires” the proboscis inside out to attack prey (McDermott, 1985). One type of proboscis exits from a pore that is separate from the mouth and entangles and immobilises prey with sticky, venomous secretions. A different kind of proboscis exits from the mouth and typically has a calcareous barb called a stylet to stab prey and inject it with venom and digestive fluids. Prey can then be swallowed whole, or its tissues may be sucked into the mouth.

Five-lined ribbon worm (Baseodiscus quinquelineatus).
Pink ribbon worm, possibly Gorgonorhynchus species.

Phylum Nematoda

Nematodes, aka the roundworms, are estimated at around 25,00 species (Hodda, 2011), although others estimate this number to be over the 1 million mark (Lambshead, 1993). They are regarded as pseudocoelomates as they have a fluid-filled cavity between the digestive tract and the body wall, although it is not lined with tissue, and there is no membrane-like tissue supporting the organs and, therefore, is not a true coelom. They have a complete digestive system and an external, collagenous cuticle, which is shed usually four times before reaching adulthood; just before the moult, the old cuticle is softened by enzymes that accumulate between the old and new cuticle until the old one is shed.

Microscopic, transparent, terrestrial roundworms (Caenorhabditis elegans), usually around 1mm in length and found in temperate, soil environments.

Phylum Annelida

I like to refer to annelids as your classics. They’re what you imagine when you hear the word “worm”, but they also include over 22,000 species of ragworms, earthworms, and even leeches. Between the lot of them, they have occupied a variety of niches, including tidal zones, hydrothermal vents, freshwater, and your backyard! Marine annelids have a range of habitats, life histories, and feeding strategies, making them a critical component of the oceanic ecosystem (Capa & Hutchings, 2021).

Annelids are pretty advanced. They have a complete gut, a closed circulatory system with blood vessels, bilateral symmetry, cephalisation (somewhat), and usually a pair of coelomata in each segment. Annelid segmentation facilitates the specialisation of body parts into different functions. A collagenous cuticle covers their bodies but, unlike nematodes, does not moult and has setae to provide traction.

Your mate from the backyard: the humble earthworm (Lumbricina species).
A marine bloodworm (Glycera species).
A marine leech (Pontobdella muricata).

References

Capa, M., & Hutchings, P. (2021). Annelid diversity: Historical overview and future perspectives. Diversity, 13(3), 129.

Chim, C. K., Ong, R. S., & Gan, B. Q. (2015). Penis fencing, spawning, parental care and embryonic development in the cotylean flatworm Pseudoceros indicus (Platyhelminthes: Polycladida: Pseudocerotidae) from Singapore. Raffles Bulletin of Zoology, 31, 60–67.

Collins III, J. J. (2017). Platyhelminthes. Current Biology, 27(7), R252–R256.

Hodda, M. (2011). “Phylum Nematoda Cobb 1932. In: Zhang, Z.-Q.(Ed.) Animal biodiversity: An outline of higher-level classification and survey of taxonomic richness. Zootaxa, 3148(1), 63–95.

Jennings, J. B. (1957). Studies on feeding, digestion, and food storage in free-living flatworms (Platyhelminthes: Turbellaria). The Biological Bulletin, 112(1), 63–80.

Lambshead, P. J. D. (1993). Recent developments in marine benthic biodiversity reserch. Oceanis, 19, 5–24.

McDermott, J. J., & Roe, P. (1985). Food, feeding behavior and feeding ecology of nemerteans. American Zoologist, 25(1), 113–125.