List of all 15 Ephippidae species (following Nelson, 2006), with their respective trophic classification, according to the available literature. Single asterisks indicate dubious literature regarding trophic habits, suggesting both herbivorous and carnivorous habits by these species. Double asterisks indicate detritivorous habits as well. Hyphens indicate no available data on diet or feeding habits.
Ephippidae fish are commonly classified as being omnivorous, though tending to carnivore habits fishes (Burgess, 1978; Heemstra, 2001; Kuiter & Debelius, 2001). The group is broadly distributed in sub-tropical and tropical coastal regions, comprising eight genera and 16 species (Nelson, 2006), where the larger genera are
The literature concerning feeding habits and feeding behavior of ephippid fish is still very scarce. Recent studies, however, show that the trophic classification of the group is controversial. Depending on the ontogenetic stage, and on specific environmental conditions, juvenile
Misleading information regarding diet and feeding habits of
Moreover, Bellwood et al. (2006) have suggested ephippid fish as belonging to a “sleeping functional group”, where individual fish have the potential to explore algae-rich substrates for food, such as phase-shifted corals, helping with the recovering process of the latter environments, via removing the thick algae layer from whitened corals, as the observed in a few adult individuals of
The present review aims to verify if ephippid fish should be classified as a potential functional group, examining both the available literature on Ephippid fish, as well as original data on the stomach contents of juveniles and adults of five ephippid species from four locations in Japanese and Brazilian coastal waters. Feeding plasticity, feeding behavior and the Group potential on playing a functional role on these coastal environments are discussed.
2. Feeding plasticity and trophic classification of Ephippid fish
Despite being a relatively small group, information on feeding habits, feeding behavior and diet of the Ephippidae is quite limited, being available mostly from technical reports based on trawl samples or bycatch material. As both methods are often limited in sample number, the resulting literature is then sparse and confusing: While there is plenty of information on trophic habits of the two main genera,
Establishing a general classification for an entire fish group is always controversial, as feeding habits may rely on several biological aspects of a given species, as ontogenetic stage, habitat conditions during settlement, etc., according to both morphological and environmental constraints for particular sizes (Gerking, 1994; Diana, 1995; Russo et al., 2008). Even for the closely related group Acanthuridae (Holcroft & Wiley, 2008), sister-group of the Ephippidae, and generally known as an herbivore group, a few species have a mixed diet, based on both zooplankton and algae (Choat et al., 2004).
According to the literature, a general classification for the trophic habits of ephippid fish is a difficult, almost impossible task. This is especially due to the contrasting information on some taxa, indicating a very plastic diet, which may include both animal and plant-based food sources, as well as different behavioral strategies, even in supposedly specialized species, such as those of the genus
Couto & Vasconcelos Filho (1980)
|Eastern Pacific||Carnivore||Schneider (1995)|
de La Cruz Agüero et al. (1997)
|Eastern Atlantic||Carnivore||Allen (1981)|
|Indo-West Pacific||Carnivore||Masuda et al. (1984)|
Kuronuma & Abe (1988)
Lieske & Myers (1994)
|Indo-West Pacific||Omnivore**||Kuiter & Debelius (2001)|
|Indo-West Pacific||Omnivore*||Myers (1991)|
Kuiter & Debelius (2001)
Barros et al. (2008, 2011)
|Indo-West Pacific||Carnivore*||Kuiter & Debelius (2001)|
Bellwood et al. (2006)
|Indo-West Pacific||Carnivore||Myers (1991)|
|Western-Central Pacific||Herbivore**||Robins et al. (1991)|
|Western Indian||Carnivore||Fischer et al. (1990)|
Morphological attributes of the cranial anatomy of
3. Stomach contents and herbivorous habits by Ephippidae species
In this section, original data on four Ephippidae species are compared with information from the literature, to clarify the importance of herbivory for the species studied. Point surveys were held in Japanese and Brazilian waters, in order to compare diet and feeding habits of the Ephippidae occurring in the Pacific and Atlantic. Sampling was due to mid-summer 2005 to early winter 2006, in Japan, and from early summer 2008 to mid-winter 2010 in Brazil.
3.1. Sampling sites
Field sampling activities were held in the reefs off the Okinawa Archipelago, Japan (JPN); and in four sites along the Western Atlantic, all in the Brazilian coast (BR) (Fig. 1). Methods for capturing fish samples varied according to the surveyed location, using nets, spearfishing, line and hook, and direct acquisition from employed fishermen or from local markets. In Brazil, most sampling sites consisted in estuarine environments (Curuçá, Bragança and some samples from Caravelas). The Table 2 summarizes sampling activities in each of the surveyed locations, detailing respective methodologies as employed.
|Okinawa (JPN)||8.54 ± 1.07||17||Employed fishermen, using several net types and hook-and-line; local fish market for all samples from Japanese waters|
|18.33 ± 2.92||3|
|17.20 ± 2.42||3|
|Curuçá (BR)||18.61 ± 1.14||33||Cast nets; gill nets, hook-and-line|
|Bragança (BR)||15.42 ± 0.91||56||Local fish market|
|Natal (BR)||9.03 ± 1.73||4||Hook-and-line|
|Caravelas (BR)||11.86 ± 1.02||42||Gill nets; spearfishing; hook-and-line|
3.2. Stomach contents analysis
Samples were placed in ice soon after capture, and stocked frozen until analysis, when we proceeded with dissection of stomachs, by cutting above the cardiac sphincter (esophagus) and below the pyloric sphincter (large intestine). An incision was made along the longitudinal axis, with contents removed with pincers, followed by rinsing the inner cavity with 70% ethanol. After rinsing and sorting, contents were identified to the lowest possible taxon. We proceeded with the analysis, using the protocol as adapted from Lima-Junior & Goitein (2001), which consists basically in calculating an index for Absolute Importance (AI) for each food item (
The absolute importance index A
where Mi is the mean of ascribed points for i. After assessing Mi values, Vi can be calculated as
where 25 is a constant of multiplication.
The results were compared with those available in the literature, to any of the surveyed species, plus relevant data on herbivory activities by any Ephippidae. Information on diet and feeding habits by juvenile
Our results for both
The greatest evidence for feeding on benthic animal prey were shell fragments, polychaetes and bryozoa, frequently observed in the stomach contents of all four species. Sand fragments as found in stomachs of both Brazilian and Japanese samples would also indicate feeding on a benthic environment, but it is not necessarily an excluding factor, as sand grains occasionally occur on weeds from shallow or turbulent environments.
Our data contrast with the most as available in the literature regarding trophic classification of the Ephippidae. While most of the literature dealing with
4. Functional role vs. feeding plasticity in Ephippidae
4.1. Effects of herbivore functional groups on habitat
Herbivory by fishes is a wide-ranging subject, and aspects of behavioral ecology and diet have been addressed since early records (Hiatt & Stratsburg, 1960; Jones, 1968; Borowitzka, 1981; Lewis, 1985), whereas functional ecology has been approached more recently (Bellwood et al., 2002; Bonaldo et al., 2011; Kopp et al., 2012). Efforts concerning herbivory by fishes have been made available in the literature, especially those regarding herbivory in recovery from damage (Bellwood et al., 2004; Ctanovic & Bellwood, 2009; Green & Bellwood, 2009). Intense herbivory activity reduces competition for space between corals and algae, herbivorous fish are widely recognized as a critical functional group on coral reefs. Herbivore fish families such as Acanthuridae and Scaridae are most prominent in this functional group, due to their broad distribution over tropical regions and their dense populations in such habitats (Francini-Filho et al., 2010), although many other fish groups dwelling coral reef environments may play a similar role (Ctanovic & Bellwood, 2009).
4.2. Herbivory by Ephippidae
General biology of ephippid fish is still a matter of controversy. Juveniles of the most species are cryptic, usually mimetic, dwelling coastal environments, and generally solitary, whereas adults usually form huge shoals, migrating over long distances, in up to 30m deep environments (Kuiter & Debelius, 2001; Nakabo, 2002). While there are a few reports focusing on juvenile mimic biology (Breder, 1942; Randall, 2005b; Barros et al., 2008; 2011), studies concerning adult biology, especially behavioral ecology, are rare. Why do adult fish form such shoals is therefore unknown, yet some authors suggest migratory shoaling as for reproductive reasons (Kuiter & Debelius, 2001). In coastal environments, such as coral reefs and estuaries, late juveniles and adults of the genera
|Gastropoda (shell fragments)||23.42||5.18||121.45|
Gerking (1994) has stated that no adult herbivorous fish are obligate plant eaters, selectively excluding all animal food from the diet, as larval herbivorous fish are often recorded to feed on algae plankton for an initial short period, then switching into zooplanktivory. After having developed all morphological and physiological characters, fish do shift back into herbivorous habits. However, for those groups usually classified as herbivorous, animal food items in the gut contents are considered rare, and often referred as incidentally ingested while fish are grazing. Despite our present results suggest herbivory as a major foraging tactic for all analyzed species, considering all-pooled data, animal protein input is still as important as algae ingestion, especially for
Although no field observations of feeding were made in Japan, our results for
Even for a limited number of individuals for both genera, our results suggest herbivory as the main feeding habits of ephippid fish, conflicting with the reports of a more carnivorous diet. Unless batfishes and spadefishes have been misclassified as carnivores, our data seems to be exceptional. Our results as presented here, supported by morphological data (Gregory, 1933) and behavioral data on both
To corroborate the predictions of Bellwood et al. (2006), we strongly recommend further
Thanks are due to Y. Masui (Blue-7-Sea) and the Chatan fishermen cooperative, in Okinawa, Japan; the fishermen community of the Cassurubá extractivist reserve, in Bahia, Brazil. We are also thankful to all members of the Laboratory of Aquatic Resources), especially S. Kamura (Hiroshima University) U. Scofield and L. Rabelo (CEPENE); J. Neto (ICMBio); R. L. Moura, R. Francini-Filho and E. Marocci (Conservation International) in Caravelas, Brazil; J. Meirelles and C. Cardoso (I. Peabiru) in Curuçá, Brazil, due to all logistic support. We are deeply grateful to H. Higuchi (MPEG) for reviewing and proofreading the manuscript. Thanks are also due to the Brazilian Council for Research and Development (CNPq, Grant #141225/2008-4), the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES, Process #6718-10-8), and the Ministry of Education, Culture, Sports Science and Technology of Japan (MEXT) for financial support.