Philippa Kaur

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A number of studies have assessed meat sourced from wild deer originating from various countries (i.e.11,12 from Poland or13 from South Africa) or from farmed deer (i.e.14 from Czech Republic11,15, from Poland16, from Italy and17from SP). Studies have also examined the main marketed deer meats: meat from wild SP deer1,2,10 and farmed NZ ones6,7,8,18. Despite the number of studies cited below which assess meat quality from different countries or different types of breeding/killing (wild or farmed, stressful or sudden death), they have been undertaken by different research teams, using different scientific equipment and protocols. None of these studies have assessed meat samples from different countries with the same scientific equipment, reagents, and staff. It is therefore likely that some of the anomalies found through comparison of the available literature may actually be caused by methodological rather than regional differences per se.
The quality of wild game meat depends on the hunting method19 and on the hunting season3. Wild deer shot with a projectile (e.g. a bullet) are not exsanguinated immediately after their death and often several hours elapse between death and dressing. Consequently, carcasses are often processed once rigor mortis has set in, which affects meat characteristics. In principle, a low stress death by stalking should result in a better quality of meat and, in fact, meat-processing companies pay better prices for meat from stalked animals than for stress hunted meat, as evidenced by game estate owners and personal interviews. Studies have assessed several types of hunted and farmed venison, but none included stressful pursuit by dogs. Our results show for the first time that the mixed effects of hunting type-season resulted in some differences in meat quality (pH, cooking losses), but surprisingly not in tenderness (shear force).
Recently, Stanisz et al.3 have not observed differences for body weight with hunting season of hunt-harvested does. However, the authors observed a higher technological quality for venison obtained in winter showing compared to that harvested in summer. In fact, it was observed lower purge loss in vacuum, drip loss, free water, free water share in total water, and water loss during roasting. In addition, venison obtained in winter showed a greater brightness and a reduced redness comparing to venison obtained in summer. Colour traits and water retention capacity determine the meat shelf life and its suitability for storage in vacuum packaging.
Values obtained in the current study for pH of meat were similar to those observed previously for meat from NZ farmed deer7,9 and for SP stressed, hunted red deer2,10. However, no data has been found to compare the average values of pH obtained in SP from stalked deer. Our results show that pH values were similar for wild deer in SP (pooled values) and farmed deer in NZ, but meat from stalked deer had the lowest values. This is not surprising as transporting deer to the abattoir also involves stress, and furthermore, recently, Gentsch et al.20 have observed that cortisol levels for stalked deer were much lower than those for deer hunted with dogs in driven hunts (21.8 vs. 66.1 nmol/L, respectively). With regard to the effect of seasons, meat hunted in winter had a higher pH than meat hunted in summer. However, recently, Stanisz et al.3 observed that the pH of the muscles Longissimus lumborum measured 24 h post-mortem was 0.22 units higher in the summer season, compared to the winter season. This is consistent with current results regarding colour and literature reports that pre-harvest stress affects the degree of bleed, leading to an increase in the level of oxymyoglobin21 and confirming the influence of hunting type on meat colour4. According to results obtained by Stanisz et al.3, venison sourced from does shot in summer was redder and had a greater chroma compared to venison obtained in winter. In our study, values obtained for colour traits were similar to those obtained for NZ farmed6,9 and for SP stress hunted10 deer meat.
The IMF content was similar to the values previously reported for NZ farmed deer8,9 and for autumn–winter hunted deer from the same region of SP1,10. However, the most interesting information came from slight differences in IMF between seasons/type of hunting in wild SP: meat from summer stalking had an average IMF content of 0.90%, a value significantly higher than that for winter chased meat (0.11%). This may be only a seasonal difference (unlikely to be attributable to stress at death) because of increased grazing available during spring and summer for the deer. Thus, it is well established that body condition of deer improves, mainly in gaining fat and body weight, during spring and summer. In contrast, loss condition, involving loss of body fat, is higher in autumn and winter22. In addition, deer lose weight in autumn because feed intake decreases considerably during the rut23. Confirming this hypothesis, Serrano et al.2 have found higher contents of IMF and cholesterol in the loin of deer hunted in driven hunts in autumn compared to the loin from deer hunted in driven hunts in winter. The cooking losses of meat were similar to values reported previously for NZ farmed deer7 and for stressed deer hunted in driven hunts in SP10, although there was an effect of stress/season with values higher for stalking-summer. The effect of season on cooking losses has been previously described3. However, the cause of the differences observed in current study is likely to be due to the level of stress at slaughter, corroborated by Cifuni et al.4, who found that meat from culled (selective hunting) deer produced a greater degree of water loss during cooking than meat from deer slaughtered in driven hunts.
In general, values reported for shear force present a high variability2,12,13. Values in the current trial were higher than those reported previously for deer meat1,8,9,10. Differences among authors might be due to a range of interrelated factors, including pH, amount of connective tissue, IMF content, proteolytic enzyme activity and age of the animal13. Differences observed for the shear force between countries of origin (58.7% higher for meat from SP than for NZ meat) are not caused by stress at death: no differences were observed regarding the shear force of SP meat by hunting type/season. In fact, Stanisz et al.3 concluded that a greater impact of season could be evidenced using biting measures (Volodkevich Bite Jaws, test speed 2 mm/s; strain 100%; force 5 g at 24 h and 14 days post-mortem) compared to Warner–Bratzler measures. However, biting measures were not included in the current study. Further studies may be needed to conclude whether there is an effect of season compensating for the apparent effect of stress that yields non-significant results.
In general, the country of origin did not influence the total content of SFA or PUFA and a trend was only detected in the increase of the MUFA content of NZ meat. However, meat from NZ farms had higher content of n-3 FA and long chain n-3 PUFA, less content of n-6 FA and, in consequence, a lower n-6/n-3 ratio than SP wild meat. Values obtained for the n-6/n-3 ratio (ranging from 1.22 to 3.71) correspond with those reported by other authors for deer meat8,14. In any case, the average n-6/n-3 ratio for meat from both countries of origin was lower than 4, as recommended by WHO/FAO24.
The FA profile differed for meat samples obtained by different hunting types/season. The differences observed in the current study between hunting types for the FA profile are likely to be caused by the effects of the diet FA profiles seasonal changes on ruminant products25. Thus, the main FA in winter driven hunt meat were PUFA, followed by SFA and MUFA. In summer stalked deer and farmed venison, the main FA were SFA followed by MUFA and PUFA. No differences were observed for the contents of n-3 FA. Consequently, the fat of animals sourced from driven hunts in winter showed a higher PUFA/SFA ratio, n-6 FA content and n-6/n-3 ratio than the fat of summer stalked deer.
In general, the AA profile obtained in this study corresponds with that reported for meat from red deer, as previously indicated by Lorenzo et al.1. Interesting effects of country of origin and hunting type on AA profile of deer meat were observed in the current study. The SP wild meat had higher contents of total, essential and non-essential AA than NZ farm meat. Moreover, meat collected from summer-stalked deer presented a higher ratio for the essential/non-essential AA than meat collected from deer slaughtered in winter driven hunts. However, authors have not found previous studies comparing the AA profile of meat from SP and NZ deer slaughtered by different methods to compare with current results. It is postulated, therefore, that AA differences are attributable to seasonal effect, not the level of stress at death.
Because mineral composition presented in deer meat is closely related to the natural environment as they graze and browse26, differences found in mineral content in our study seem to depend on season and diet composition rather than on level of stress at death. Therefore, the differences in fodder available in spring and summer as compared to winter, as well as the growth of leaves in deciduous trees and shrubs, may explain some of the differences in the mineral profile observed between meats sourced from winter driven hunts and summer stalking analysed in the current study. Actually, Estévez et al.27 found seasonal differences in the mineral content of plants consumed by deer in SP. It is highly unlikely that mineral differences between both meats are due to the level of stress at death: the only difference that could be expected (Na content) due to increased sweating resulting from the chase and stress, was actually the reverse of what was expected (greater in animals killed in winter driven hunts). These results suggest that the difference was due to a lower level of Na in plants in summer.
One of the most significant effects in the seasonal differences found in the current study may not be related to mineral content of the diet, but to another very interesting and unique physiological characteristic of male deer (the sex examined in this study): cyclic physiologic osteoporosis. This effect is caused by rapid growth of the antlers (more than 1 cm/day), causing a depletion of mineral stores in certain bones in order to transfer the material to antlers28. Because minerals are blood borne, it is not surprising that they may also affect the mineral composition of muscles. This could explain why meat from osteoporotic deer (summer) had less than half the content of Zn, which forms part of alkaline phosphatase, the enzyme needed to deposit Ca in bone tissue29. For the same reason, it may explain the differences found for P and Ca contents (despite Ca is more stable in blood), and even for Mg (which can substitute Ca in the hydroxyapatite forming the antlers and bones). More

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National Institute of Water and Atmospheric Research, Hataitai, New Zealand
Jade Maggs

Endangered Marine Species Research Unit, Borneo Marine Research Institute, Universiti Malaysia Sabah, Kota Kinabalu, Malaysia
B. Mabel Manjaji-Matsumoto

Department of Marine Biology, Texas A&M University at Galveston, Galveston, TX, USA
Philip Matich

Aquarium of the Pacific, Long Beach, CA, USA
Erin McCombs

Khaled bin Sultan Living Oceans Foundation, Annapolis, MD, USA
Llewelyn Meggs

Department of Biodiversity, Conservation & Attractions, Parks & Wildlife WA, Pilbara Region, Nickol, Western Australia, Australia
Stephen Moore

Large Marine Vertebrates Research Institute Philippines, Jagna, The Philippines
Ryan Murray & Alessandro Ponzo

Wasage Divers, Wakatobi and Buton, Indonesia
Muslimin Kaimuddin

Western Australian Fisheries and Marine Research Laboratories, Department of Primary Industries and Regional Development, Government of Western Australia, North Beach, Western Australia, Australia
Stephen J. Newman & Michael J. Travers

Island Conservation Society Seychelles, Victoria, Mahé, Seychelles
Josep Nogués

CORDIO East Africa, Mombasa, Kenya
Clay Obota & Melita Samoilys

The Centre for Ocean Research and Education, Gregory Town, Eleuthera, Bahamas
Owen O’Shea

Department of Environment and Geography, University of York, York, UK
Kennedy Osuka

Center for Fisheries Research, Ministry for Marine Affairs and Fisheries, Jakarta Utara, Indonesia
Andhika Prasetyo

Universitas Dayanu Ikhsanuddin Bau-Bau, Bau-Bau, Indonesia
L. M. Sjamsul Quamar

Pristine Seas, National Geographic Society, Washington, DC, USA
Enric Sala

Department of Zoology, University of Oxford, Oxford, UK
Melita Samoilys

HJR Reefscaping, Boquerón, Puerto Rico
Michelle Schärer-Umpierre

SalvageBlue, Kingstown, Saint Vincent and the Grenadines
Nikola Simpson

School of Natural and Computational Sciences, Massey University, Auckland, New Zealand
Adam N. H. Smith

Indo Ocean Project, PT Nomads Diving Bali, Nusa Penida, Indonesia
Lauren Sparks

Manchester Metropolitan University, Manchester, UK
Akshay Tanna & Alexandra M. Watts

Reef Check Dominican Republic, Santo Domingo, Dominican Republic
Rubén Torres

Institut de Recherche pour le Développement, UMR ENTROPIE (IRD-UR-UNC-CNRS-IFREMER), Nouméa, New Caledonia
Laurent Vigliola

Secretariat of the Pacific Regional, Environment Programme, Apia, Samoa
Juney Ward

Department of Life Science, Tunghai University, Taichung, Taiwan
Colin Wen

School of Environmental and Forest Sciences, University of Washington, Seattle, WA, USA
Aaron J. Wirsing

Corales del Rosario and San Bernardo National Natural Park, GIBEAM Research Group, Universidad del Sinú, Cartagena, Colombia
Esteban Zarza-Gonzâlez

D. Chapman and M. Heithaus conceived the study with assistance from M. Heupel, C.A.S., M.M., E.H. and M.A.M. D. Chapman, M. Heithaus, M. Heupel, C.A.S., M.M. and E.H. directed fieldwork run by J.G., J.K., M.E.B., L.M.C.-R., C.W.S., K.I.F., J.V.-A., G.C. and C.S.S. Database management was by T. Gorham. M.A.M. and D. Chapman drafted the manuscript, with help from M. Heithaus, M. Heupel, C.A.S., J.E.M.C., M.M., E.H., J.G., J.K., M.E.B., L.M.C.-R., C.W.S., C.S.S., M.J.R., V.U. and T. Gorham. All other authors contributed equally, made substantial contributions to data collection, provided input and approved the text in the manuscript. More

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The lignite mine at Bełchatów, Central Poland (Fig. 1), has recently yielded abundant Miocene remains of several species of branchiopod microcrustaceans. They pertain to the order Anomopoda or water fleas, families Chydoridae and Bosminidae. The main synapomorphy of the anomopods is the ephippium, a structure in which sexual or resting eggs are deposited and that forms when external conditions deteriorate. The Daphniidae include the well-known and speciose genus Daphnia, a highly specialized pelagic component of the freshwater zooplankton. The ephippium fossilizes well and is mostly the only structure that survives as a fossil. The Chydoridae are mostly found in the littoral of lakes and ponds, among water plants. The Bosminidae are pelagic, like Daphnia, but are much smaller (around 0.5 mm in body size) while Daphnia and other daphniids may reach up to 6–7 mm.
Figure 1

(A) View of the Bełchatów Lignite Mine outcrop (photo from the nineties of the twentieth century, when the material was collected). The sedimentary unit with deposits with the cladoceran fossils is to the lower right of the picture (photo: G. Worobiec). (B) Piece of mudstone with cladoceran remains (Collection KRAM-P 225, stored in the W. Szafer Institute of Botany, Polish Academy of Sciences). On the exposed surface leaves of trees and shrubs as well as the water plant Potamogeton (red circle) are seen (photo: A. Pociecha).

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The fossil-bearing deposits belong to a clayey-sandy (I-P) unit considered to be of mid to late Miocene age1,2. Beside by geology, this age is supported by fission track dating, and fossils of different animal (mollusks, fish) and plant (higher plants, water plants and algae) groups1,2,3,4,5,6,7. The fission track ages were 16.5 to 18.1 million years, while the Miocene, also known as the age of mammals, extended from 23 to 5.3 million years BP.
The Branchiopoda (a class of the Crustacea composed ten extant orders) include some of the most ancient extant crustaceans (the Anostraca or fairy shrimp) with several credible fossils8. However, the fossil record is patchy. While the oldest known anostracan-like representatives date back to the Cambrian, fossils of the four extant so-called cladoceran orders, with an estimated 1,000 extant species, is poor9 and somewhat paradoxical. The order Ctenopoda is known from ca 60 extant species and several Mesozoic fossils (possibly representing orders in their own right) but is rare in the most abundant source of fossils, the sediments of late Pleistocene–Holocene lakes10,11. The Anomopoda, in contrast, have to date a limited Mesozoic fossil record, but their subfossils abound in Holocene lake sediments.
The family Chydoridae is represented in Bełchatów by at least four genera: Alona, Acroperus, Camptocercus, and Chydorus. Alona s.l. rivals Daphnia as the most species-rich genus of the order9. All Alona fossils seen so far had two connected head-pores (Fig. 2), placing them near or in the somewhat controversial genus Biapertura. In modern European faunas, and except for Biapertura affinis, three-pored species are dominant, while two-pored ones tend to be typical of warm-climate faunas. The postabdomen, another typical anomopod structure functioning more or less as a ‘tail’, is similar but not identical to that of Biapertura affinis. Furthermore, distinct other species (Fig. 2) have been found as well.
Figure 2

Alona with two head pores from Miocene mudstone from Bełchatów [(A–C), headshields; (B) arrow, labrum; (D, F, G, H) abdomens; (E) shell with abdomen] (photo: A. Pociecha, E. Zawisza).

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Another type of fossils (Fig. 3) shares characters of the genera Acroperus and Camptocercus. Some body parts suggest the presence of Acroperus cf. harpae, others are Campocercus like. One three-dimensional fossil of a first trunk limb (P1) with soft parts preserved shows an IDL (inner distal lobe) with two setae and a moderately well developed claw. In Acroperus, a seta instead of a claw is found here. In Camptocercus, P1 has a big hook here, and our fossils are therefore intermediate between both genera, suggesting the fossil to belong to an extinct ancestral stage. The genus Chydorus is represented by C. sphaericus-like fossils (Fig. 3), but the postabdomen is needed to decide on its taxonomic status.
Figure 3

Acroperus-Camptocercus from Miocene mudstone at Bełchatów [(A) complete animal with shell, headshield, and first antenna; (B) abdomen; (C) shell; (D) claw; (E) shell with abdomen; (F) headshield with soft parts, viz. first and second trunk limbs with IDL setae conserved] (photo: A. Pociecha, E. Zawisza).

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Significantly, Bosminidae in our material were almost as abundant as Alona, while in this family no pre-Pleistocene fossils were previously known at all. Most body parts have been recovered (Fig. 4), but not the postabdomen, which is diagnostic. There is strong variation in the fossils, like in the length of the first antenna (compare Fig. 4B with Fig. 4C,E) and the posterior mucro of the valve. It is impossible to decide whether these antennae belong to several or to a single cyclomorphotic species. However, the distinctly swollen mucros like in Fig. 4A, arrow, are not known in any modern Bosmina, and suggest an extinct taxon.
Figure 4

Bosmina from Miocene mudstone from Bełchatów [(A, D, F) shell; (B) shell with headshield; (C) headshield with first antenna; (E) first antenna)] (photo: A. Pociecha, E. Zawisza).

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Daphniid fossil evidence goes back to the Jurassic/Cretaceous boundary. Fossils are fairly common but only consist of resting eggs (ephippia). Ephippia can tentatively be identified to genus level, which has led to the idea that the two subfamilies of Daphniidae have been around, apparently unchanged, for more than 140 million years9. This is known as the morphological stasis hypothesis. Its factual basis is weak although we accept that true Daphnia ephippia occur in the cretaceous of China, Mongolia and Australia9. Credible ephippia have also been isolated from Eocene age Messel pit-oil shales11. Moina (a water flea related to Daphnia) ephippia have been recovered from the early Miocene Barstow formation12,13,14. In the latter place, fossils are three-dimensional, like in our case in Bełchatów. It should be emphasized, however, that at Bełchatów no daphniid fossils have to date been discovered.
A variety of plant and animal groups, including water plants like Potamogeton have been documented from the Bełchatów site. Many are as beautifully preserved as the cladocerans3,4,5,6,7 and attempts have been made to reconstruct the climatic environment in which they lived. It is suggested to have been warmer than today (average 13.5°–16.5°C, cooling down gradually towards the end of the Miocene). The water was probably slowly flowing, through what may have been a swamp or a group of oxbow lakes from freshwater ecosystems2,15.
That we recovered no daphniid fossils may refine our insight into the nature of the Bełchatów aquatic environment: We favour the idea of a series of shallow oxbow lakes in a climate warmer than todays, with at least locally an abundance of macrophytes. Chydorids thrive in such environments, and the genus Simocephalus among daphniids also prefers such an environment. Simocephalus is quite common and widespread in modern weedy lakes but it has not been found in Bełchatów either. Like Daphnia, Bosminids are truly planktonic and need open water. Therefore, the Bełchatów lakes were probably a patchwork of macrophyte beds and open water.
So where did all the daphniids go? Daphniids are also relatively large species (up to several mm in size), while chydorids and bosminids are typically below a millimeter in size. This suggests size-selective predation on the zooplankton, most probably by fish16. Fish (tench, pike, and unidentified species) were present at Bełchatów4, at least until the middle Miocene. Tench is an omnivore and Pike is zooplanktivorous in its early stages, turning to piscivory in later life. Predation-driven exclusion of these large cladocerans may therefore well have acted in concert with the physical environment.
Predatory exclusion is seldom absolute, especially in a non-tropical climate with a cold season (‘winter’) during which predation is relaxed. This allows the prey to recover. In Bełchatów, we see no such a recovery, so another factor must have intervened. We suggest this may have been linked to water chemistry. Cladocerans, though of worldwide occurrence, are sensitive to water chemistry, more than the copepods, the second main group making up the zooplankton. We are unable to specify the precise nature behind the chemical exclusion of daphniids, but there are many examples of lakes in which Cladocera are chemically depressed. Sometimes, like in Lake Tanganyika (Africa), and the Mallili lakes (Indonesia), Cladocera are excluded altogether17,18.
In conclusion, our Miocene assemblage significantly expand our insights in anomopod evolution. They resemble modern faunas but at the same time show stronger signs of evolution at the species and at the genus level than expected under the morphological stasis hypothesis based on Daphnia ephippia. We also find clear indications of a species diversity that resembles todays’, with morphologies that look familiar at first sight but prove divergent in the details.
Bosminid fossils used to be known from the Pleistocene only, but in the Bełchatów fauna they are remarkably abundant and some of them show an unfamiliar morphology. This is best interpreted as a case of paleo-competitive release. Daphniids normally dominate the pelagic and keep bosminid abundances down. But their absence gives these small crustaceans a chance to prosper and dominate the open waters. More

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