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Juvenile‐to‐adult transition invariances in fishes: Perspectives on proximate and ultimate causation

Journal of Fish Biology

July 2022
101(4)

DOI:10.1111/jfb.15146

Authors:

Daniel Pauly

University of British Columbia

To bridge physiological and evolutionary perspectives on size at maturity in fishes, the authors focus on the approximately invariant ratio between the estimated oxygen supply at size at maturity (Qm) relative to that at asymptotic size (Q∞) among species within a taxonomic group, and show how two important theories related to this phenomenon complement each other. Gill‐oxygen limitation theory proposes a mechanistic basis for a universal oxygen supply‐based threshold for maturation, which applies among and within species. On the contrary, the authors show that a generalisation of life‐history theory for the invariance of size at maturity (Lm) relative to asymptotic size (L∞) can provide an evolutionary rationale for an oxygen‐limited maturation threshold (Qm/Q∞). Extending previous inter‐ and intraspecific analyses, the authors show that maturation invariances also occur in lake whitefish Coregonus clupeaformis (Mitchill 1818), but at both scales, theory seems to underestimate the value of the maturation threshold. They highlight some key uncertainties in the model that should be addressed to help resolve the mismatch.

A concept map showing the basic structure of metabolic models of growth and maturity (left‐hand side) and evolutionary models of growth and maturity (right‐hand side). On the left, the environment sets the parameters of metabolic models, which then determine a life history. On the right, the environment sets the selection factors which determine an optimal life history. The proximate and ultimate approaches are linked through a shared environment and because metabolic models can feed into life‐history model as parameters

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The relationship between optimal R (Lm/L∞) and h for different values of (a) d and (b) b, where h describes the trade‐off in the K–L∞ relation (L∞ ∝ K−h/δ), d is the scaling exponent of anabolism and b is the exponent in the length–mass relationship. Fish are expected to mature at a smaller size relative to asymptotic size with a more severe trade‐off (larger h), greater oxygen supply (larger d) or a smaller b

…

The relationship between estimated L∞ raised to the power of δ and estimated size at 50% maturity (Lm) raised to the power of δ among 25 populations of Coregonus clupeaformis by sex. The blue line shows the 0‐intercept regression for females (blue triangles); a green line for males (green squares) is hidden under the blue line. For comparison, the black dots show data from Pauly (1984) with the solid black line showing the 0‐intercept line with a slope of 1.361. The dotted black line shows the 1:1 relationship

…

The relationship between δln(L∞) and ln(K) among 25 Coregonus clupeaformis populations by sex (females = blue squares, males = green triangles). Also shown are the linear relationships estimated from standardised major axis regression

…

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REGULAR PAPER

Juvenile-to-adult transition invariances in fishes:

Perspectives on proximate and ultimate causation

Yolanda E. Morbey

| Daniel Pauly

Department of Biology, Western University,

London, Ontario, Canada

Institute for the Oceans and Fisheries,

University of British Columbia, Vancouver,

British Columbia, Canada

Correspondence

Yolanda E. Morbey, Department of Biology,

Western University, 1151 Richmond St. N,

London, ON N6A 5B7, Canada.

Email: ymorbey@uwo.ca

Abstract

To bridge physiological and evolutionary perspectives on size at maturity in fishes,

the authors focus on the approximately invariant ratio between the estimated oxygen

supply at size at maturity (Q

) relative to that at asymptotic size (Q

∞

) among species

within a taxonomic group, and show how two important theories related to this phe-

nomenon complement each other. Gill-oxygen limitation theory proposes a mecha-

nistic basis for a universal oxygen supply-based threshold for maturation, which

applies among and within species. On the contrary, the authors show that a generali-

sation of life-history theory for the invariance of size at maturity (L

) relative to

asymptotic size (L

∞

) can provide an evolutionary rationale for an oxygen-limited mat-

uration threshold (Q

∞

). Extending previous inter- and intraspecific analyses, the

authors show that maturation invariances also occur in lake whitefish Coregonus

clupeaformis (Mitchill 1818), but at both scales, theory seems to underestimate the

value of the maturation threshold. They highlight some key uncertainties in the

model that should be addressed to help resolve the mismatch.

KEYWORDS

gill-oxygen limitation theory, growth models, life-history theory, size at maturity invariance

1|INTRODUCTION

In aquatic environments, dissolved oxygen is a key physical parameter

affecting the physiology, performance, survival and distribution of

organisms (Ficke et al., 2007;Pörtner,2001;Pörtner&Knust,2007;

Wu, 2002). In fishes, oxygen plays an important role in driving trends in

growth and body size (Atkinson, 1994), and oxygen limitation has been

implicated as a mechanism underlying fish size declines because of cli-

mate warming and commercial fisheries (Baudron et al., 2014;

Pauly, 2019; Pauly & Cheung, 2017;vanRijnet al., 2017;Waples&

Audzijonyte, 2016). Changes in oxygen supply and demand during

ontogeny may also influence the size at which fish sexually mature, as

proposed by Pauly (Pauly, 1984,2021a,2021b), and shown by experi-

ments on Nile tilapia Oreochromis niloticus (L. 1758) (Kolding

et al., 2008) and guppies Poecilia reticulata Peters 1859 (Diaz Pauli

et al., 2017). Yet oxygen supply and demand as a determinant of fish

growth, body size and maturation has stimulated fierce debate

between its critics (e.g., Lefevre et al., 2017,2018) and its proponents

(Pauly, 2021a; Pauly & Cheung, 2017,2018). Recognising the impera-

tive to address issues related to global change in aquatic environments

and to move beyond this stalemate, the authors’aim was to show that

oxygen-limited maturation is consistent with an evolutionary perspec-

tive as embodied by life-history theory (LHT).

The study of life histories, which refer to the time course of

development, growth, survival and reproduction, can be roughly

divided into studies of proximate vs. ultimate causation. Extending

early discussion of proximate vs. ultimate causation in the context of

animal behaviour by Tinbergen (1963,2005), proximate mechanisms

include the genetic, ontogenetic, physiological, ecological and beha-

vioural processes that occur within the lifetime of an individual to pro-

duce a life history of a particular form. Physiologists, ecologists and

ethologists generally focus on experimental evidence and will often

overlook the nuances of adaptive function (i.e., fitness value). On the

contrary, evolutionary and behavioural ecologists generally focus on

the underlying adaptive function of a specific life-history combination.

They will often rely on evolutionary models and will usually simplify

Received: 15 March 2022 Accepted: 24 June 2022

DOI: 10.1111/jfb.15146

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Nov 2020

Michael R Kearney

Metabolic theory aims to tackle ecological and evolutionary problems by explicitly including physical principles of energy and mass exchange, thereby increasing generality and deductive power. Individual growth models (IGMs) are the fundamental basis of metabolic theory because they represent the organisational level at which energy and mass exchange processes are most tightly integrated and from which scaling patterns emerge. Unfortunately, IGMs remain a topic of great confusion and controversy about the origins of the ideas, their domain and breadth of application, their logical consistency and whether they can sufficiently capture reality. It is now 100 years since the first theoretical model of individual growth was put forward by Pütter. His insights were deep, but his model ended up being attributed to von Bertalanffy and his ideas largely forgotten. Here I review Pütter's ideas and trace their influence on existing theoretical models for growth and other aspects of metabolism, including those of von Bertalanffy, the Dynamic Energy Budget (DEB) theory, the Gill‐Oxygen Limitation Theory (GOLT) and the Ontogenetic Growth Model (OGM). I show that the von Bertalanffy and GOLT models are minor modifications of Pütter's original model. I then synthesise, compare and critique the ideas of the two most‐developed theories, DEB theory and the OGM, in relation to Pütter's original ideas. I formulate the Pütter, DEB and OGM models in the same structure and with the same notation to illustrate the major similarities and differences among them. I trace the confusion and controversy regarding these theories to the notions of anabolism, catabolism, assimilation and maintenance, the connections to respiration rate, and the number of parameters and state variables their models require. The OGM model has significant inconsistencies that stem from the interpretation of growth as the difference between anabolism and maintenance, and these issues seriously challenge its ability to incorporate development, reproduction and assimilation. The DEB theory is a direct extension of Pütter's ideas but with growth being the difference between assimilation and maintenance rather than anabolism and catabolism. The DEB theory makes the dynamics of Pütter's ‘nutritive material’ explicit as well as extending the scheme to include reproduction and development. I discuss how these three major theories for individual growth have been used to explain ‘macrometabolic’ patterns including the scaling of respiration, the temperature–size rule (first modelled by Pütter), and the connection to life history. Future research on the connections between theory and data in these macrometabolic topics have the greatest potential to advance the status of metabolic theory and its value for pure and applied problems in ecology and evolution.

On confusing cause and effect in the oxygen limitation of fish

Article

Jul 2018

Given ocean warming, the GOLT predicts a reduction of the size of fish due to their inability to compensate, via their gill surface, for the increased metabolic rate that results from higher temperatures (Cheung et al., 2013). Lefevre et al. (2017, 2018) objected to this because they believe that fish can grow gills as needed, such that oxygen supply cannot be limiting their metabolism. Pauly & Cheung (2017) responded to this claim, refuted its various elements, and reiterated the basic dimensional argument that is at the basis of the GOLT. This article is protected by copyright. All rights reserved.

Juvenile‐to‐adult transition invariances in fishes: Perspectives on proximate and ultimate causation

Abstract and Figures

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