Johanna Werminghausen

Presence of cleaner wrasse increases the recruitment of damselfishes to coral reefs.

Mutualisms affect the biodiversity, distribution and abundance of biological communities. However, ecological processes that drive mutualism-related shifts in population structure are often unclear and must be examined to elucidate how complex, multi-species mutualistic networks are formed and structured. In this study, we investigated how the presence of key marine mutualistic partners can drive the organisation of local communities on coral reefs. The cleaner wrasse, Labroides dimidiatus, removes ectoparasites and reduces stress hormones for multiple reef fish species, and their presence on coral reefs increases fish abundance and diversity. Such changes in population structure could be driven by increased recruitment of larval fish at settlement, or by post-settlement processes such as modified levels of migration or predation. We conducted a controlled field experiment to examine the effect of cleaners on recruitment processes of a common group of reef fishes, and showed that small patch reefs (61–285 m2) with cleaner wrasse had higher abundances of damselfish recruits than reefs from which cleaner wrasse had been removed over a 12-year period. However, the presence of cleaner wrasse did not affect species diversity of damselfish recruits. Our study provides evidence of the ecological processes that underpin changes in local population structure in the presence of a key mutualistic partner.

Characterizing the ecological trade‐offs throughout the early ontogeny of coral recruitment

Drivers of recruitment in sessile marine organisms are often poorly understood, due to the rapidly changing requirements experienced during early ontogeny. The complex suite of physical, biological, and ecological interactions beginning at larval settlement involves a series of trade-offs that influence recruitment success. For example, while cryptic settlement within complex microhabitats is a commonly observed phenomenon in sessile marine organisms, it is unclear whether trade-offs between competition in cryptic refuges and predation on exposed surfaces leads to higher recruitment.To explore the trade-offs during the early ontogeny of scleractinian corals, we combined field observations with laboratory and field experiments to develop a mechanistic understanding of coral recruitment success. Multiple experiments conducted over 15 months in Palau (Micronesia) allowed a mechanistic approach to study the individual factors involved in recruitment: settlement behavior, growth, competition, and predation, as functions of microhabitat and ontogeny. We finally developed and tested a predictive recruitment model with the broader aim of testing whether our empirical insights explained patterns of coral recruitment and quantifying the relative importance of each trade-off.Coral settlement was higher in crevices than exposed microhabitats, but post-settlement bottlenecks differed markedly in the presence (uncaged) and absence (caged) of predators. Incidental predation by herbivores on exposed surfaces at early post-settlement (<3 mm) stages and targeted predation by corallivores at late post-settlement (3–10 mm) stages exceeded competition in crevices as major drivers of mortality. In contrast, when fish were excluded, competition with macroalgae and heterotrophic invertebrates intensified mortality, particularly in crevices. As a result, post-settlement trade-offs were reversed, and recruitment was more than twofold higher on exposed surfaces than crevices. Once post-settlement bottlenecks were overcome, survival was higher on exposed surfaces regardless of fish exclusion. However, maximum recruitment occurred in crevices of uncaged treatments, being ninefold higher than caged treatments. Overall, we characterize recruitment success throughout the earliest life-history stages of corals and uncover some intriguing trade-offs between growth, competition and predation, highlighting how these change and even reverse during ontogeny and under alternate disturbance regimes.

Power and temptation cause shifts between exploitation and cooperation in a cleaner wrasse mutualism

In many instances of cooperation, only one individual has both the potential and the incentive to ‘cheat’ and exploit its partner. Under these asymmetric conditions, a simple model predicts that variation in the temptation to cheat and in the potential victims capacity for partner control leads to shifts between exploitation and cooperation. Here, we show that the threat of early termination of an interaction was sufficient to induce cleaner wrasse Labroides dimidiatus to feed selectively against their preference (which corresponds to cooperatively eating client fish ectoparasites), provided that their preference for alternative food was weak. Under opposite conditions, cleaners fed selectively according to their own preference (which corresponds to cheating by eating client mucus). By contrast, a non-cleaning fish species, Halichoeres melanurus, failed to adjust its foraging behaviour under these same conditions. Thus, cleaners appear to have evolved the power to strategically adjust their levels of cooperation according to the circumstances.

Female fitness optimum at intermediate mating rates under traumatic mating.

Traumatic mating behaviors often bear signatures of sexual conflict and are then typically considered a male strategy to circumvent female choice mechanisms. In an extravagant mating ritual, the hermaphroditic sea slug Siphopteron quadrispinosum pierces the integument of their mating partners with a syringe-like penile stylet that injects prostate fluids. Traumatic injection is followed by the insertion of a spiny penis into the partner’s gonopore to transfer sperm. Despite traumatic mating, field mating rates exceed those required for female fertilization insurance, possibly because costs imposed on females are balanced by direct or indirect benefits of multiple sperm receipt. To test this idea, we exposed animals to a relevant range of mating opportunity regimes and assessed the effects on mating behavior and proxies of female fitness. We find penis intromission duration to decrease with mating rates, and a female fecundity maximum at intermediate mating rates. The latter finding indicates that benefits beyond fertilization insurance can make higher mating rates also beneficial from a female perspective in this traumatically mating species.

No effect of mate novelty on sexual motivation in the freshwater snail Biomphalaria glabrata.

BackgroundWhen mating effort (e.g. via ejaculates) is high, males are expected to strategically allocate their resources depending on the expected fitness gains from a given mating opportunity. One mechanism to achieve strategic mating is the Coolidge effect, where male sexual motivation declines across repeated encounters with a familiar partner, but resuscitates when encountering a novel female. Experimental tests of male mate choice via mechanisms such as the Coolidge effect, however, remain scarce. Moreover, it is untested to date whether the Coolidge effect occurs in a sex-specific manner in simultaneous hermaphrodites, where the motivation to mate with a familiar partner may vary with previous mating activity in the male or female role.ResultsWe exposed focal hermaphroditic freshwater snails, Biomphalaria glabrata, repeatedly to either a familiar or a novel partner. None of our proxies of sexual motivation (remating likelihood, mating delay, copulation duration) varied between the novel and familiar partner treatments. Moreover, the mating role taken during the first copulation did not affect the subsequent choice of mating roles in the familiar partner treatment as would be expected if focals preferred to avoid mating twice in the same role with a familiar partner. This indicates the absence of sex-specific effects of partner novelty.ConclusionOur data indicate that mate novelty does affect neither overall sexual motivation nor the choice of mating roles in B. glabrata. Hence, male mate choice via a Coolidge effect appears inexistent in this invertebrate hermaphrodite. We discuss the possible roles of insufficient fitness gains for discriminatory behaviour in populations with frequent mate encounters as well as poor mate discrimination capacities. Our findings lend also no support to the novel prediction that sexual motivation in simultaneous hermaphrodites varies with the mating roles taken during previous copulations, calling for empirical investigation in further hermaphrodite systems.

Cephalo-traumatic secretion transfer in a hermaphrodite sea slug

Mating rituals in the animal kingdom are often quite extraordinary, in particular when mating is traumatic. We here describe the exceptional traumatic mating behaviour of the currently undescribed sea slug, Siphopteron sp. 1. Similar to four congeners, Siphopteron sp. 1 routinely exhibits traumatic secretion transfer through a stylet-like penis appendage. Contrary to previous descriptions, however, prostate secretions are injected centrally into the partners forehead, representing, to our knowledge, the first-known instance of ‘cephalo-traumatic secretion transfer’. We further provide a comparative quantification of within- and between-species variation in injection sites and derive a potential neurophysiological function of prostate secretions that are injected close to, or into, the central nervous system.

Does traumatic secretion transfer manipulate mating roles or reproductive output in a hermaphroditic sea slug

Copulation in the simultaneous hermaphrodite Siphopteron sp. involves injection of prostate fluids into the mating partner with a stylet-shaped penile appendage before insemination. It has been hypothesised that such traumatic secretion transfer manipulates sex roles or the recipient’s short-term reproductive output. To test manipulative effects of traumatic secretion transfer, we ablated the stylet of male-acting individuals and then paired them to untreated focal individuals. Mating behaviour and egg output of focal individuals was then compared between this ‘no injection group’ and a ‘control group’ with sham-treated mating partners. We found that penile stylets were inserted at different areas prior to and during insemination, but prostate fluid injection was restricted to the first phase. Here, injections were into the anterior foot region, indicating that prostate secretions target the nearby male or female copulatory tracts. Our experimental manipulation of traumatic secretion transfer did not affect the exhibited mating roles. Matings in both treatments were usually reciprocal so that both partners acted in the male as well as female mating role. Moreover, sperm recipient reproductive output did not differ between treatments. We conclude that traumatic secretion transfer in this species either affects currently unmeasured traits, for instance the donor’s paternity share, or that these sea slugs are so well-adapted to traumatic secretion transfer that the effects were too subtle to be detected in our current assays.

Large donors transfer more sperm, but depletion is faster in a promiscuous hermaphrodite

Males are limited in sperm and seminal fluid, which can lead to prudent sperm allocation across consecutive matings. While sperm depletion is usually considered a population characteristic, we investigated an individual size-related variation in sperm depletion in the promiscuous sea slug Chelidonura sandrana. We found that sperm counts substantially declined across four successive copulations, indicating sperm depletion. Sperm depletion occurred at a disproportionally fast rate in larger sperm donors. Based on our finding of body size-dependent sperm depletion, we further investigated whether this translates into prudent sperm allocation across ejaculates. We found no evidence that slugs adjusted the number of delivered sperm in response to partner body weight, a tight proxy of fecundity. Instead, sperm counts increased with sperm donor body weight. Sperm donation independent of partner body size and—as found in previous work—partner novelty leaves scope for currently unidentified traits like the sperm competition environment to affect male sperm allocation. Alternatively, we propose that, in C. sandrana, a low optimal male mating rate close to the female optimum as indicated by our data may ultimately render indiscriminate sperm allocation the most beneficial male mating strategy.